Pathogenesis of urethral funneling in women with stress urinary incontinence assessed by introital ultrasound

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1 Ultrasound Obstet Gynecol 2005; 26: Published online 5 August 2005 in Wiley InterScience ( DOI: /uog.1977 Pathogenesis of urethral funneling in women with stress urinary incontinence assessed by introital ultrasound R. TUNN*, K. GOLDAMMER*, A. GAURUDER-BURMESTER*, B. WILDT* and D. BEYERSDORFF *Department of Urogynecology, German Pelvic Floor Center, St Hedwig Hospitals Berlin and Department of Radiology, Charité Hochschulmedizin Berlin, Germany KEYWORDS: introital ultrasound; MRI pathomorphology; stress urinary incontinence; urethral funneling ABSTRACT INTRODUCTION Objective The incidence of urethral funneling (UF) seen in women with stress urinary incontinence (SUI) during straining is reported to range from 18.6% to 97.4%. Its morphologic basis is unknown. The aim of the present study was to determine whether SUI patients with and without UF differ in terms of history, urodynamic results and magnetic resonance imaging (MRI) findings. Patients and Methods Fifty-four women (mean age 52 ± 11 years) with a history of SUI confirmed by clinical and urodynamic findings were included in the study. UF was demonstrated by introital ultrasound performed at a bladder filling volume of 300 ml during maximal straining. MRI for assessment of the urethra, levator ani muscle and endopelvic fascia was performed using axial proton-density-weighted sequences. Results UF was demonstrated by introital ultrasound in 59% of the patients with SUI (Group 1) and was absent in 41% (Group 2). There were no differences between the two groups in mean age (P = 0.208), the incidence of mild prolapse of the anterior vaginal wall (Aa, Ba; stage I; P = 0.741), and urodynamic parameters (urethral closure pressure at rest; P = 0.507). The percentages of nulliparous and parous women were 22% and 78% in Group 1 and 54% and 46% in Group 2 (P = 0.013). The two groups did not differ in the MRI demonstration of morphologic defects of the urethra, levator ani muscle and endopelvic fascia or of combined defects. Conclusions The results of the present study did not elucidate the pathogenesis of UF. The demonstration of UF crucially depends on the examination technique employed. Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd. Current theories on the origin of stress urinary incontinence (SUI) and its treatment like DeLancey s hammock hypothesis 1 and the integral theory proposed by Petros and Ulmsten 2 are highly complex and make subtle morphologic assumptions. These theoretical assumptions are in sharp contrast with the diagnostic tools available to assess SUI. Though these diagnostic modalities yield objective findings in incontinent patients, they provide only rough quantitative data that merely allow one to guess at the underlying morphologic abnormalities. This characterization also holds for introital or perineal ultrasonography performed for assessing the topography and mobility of the bladder neck, in particular for the demonstration of urethral funneling (UF) or opening of the proximal urethra while the patient is straining or coughing. The incidence of UF in women with SUI reported in the literature ranges from 18.6% to 97.4% 3 8. Comparative studies using video cystourethrography and ultrasonography have confirmed the reliability of the latter in demonstrating UF 9,10. The wide range of incidences reported is primarily due to the different conditions under which the examination is performed, e.g. whether the patient is examined in the half-sitting position or when standing (3.8% versus 27.5%) 11, or whether or not the bladder is filled with contrast medium (48.7% vs. 97.4%) 6. All studies published to date consider UF a typical finding in women with SUI, but none of the investigators has addressed the question regarding the underlying pathomorphologic cause of UF and its diagnostic implications. SUIisalsoreferredtoas vesicalizationoftheproximal urethra or bladder neck insufficiency. Both terms suggest an insufficiency of the urethral sphincter complex, but morphologic evidence for such an assumption is still Correspondence to: Dr R. Tunn, German Pelvic Floor Center, St. Hedwig Hospitals, Große Hamburger Str. 5 11, Berlin, Germany ( r.tunn@alexius.de) Accepted: 14 June 2005 Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER

2 288 Tunn et al. lacking. The present study therefore aimed at identifying differences between SUI patients with and without UF based on the patients histories, urodynamic testing, and magnetic resonance imaging (MRI) findings. If it can be shown that SUI patients with and without UF differ in terms of defects of the levator ani muscle, endopelvic fascia, and urethral defects demonstrated by MRI, the present study would establish the diagnostic relevance of UF and its potential significance for therapeutic decision making. PATIENTS AND METHODS The aim of the present study was to determine whether SUI patients with and without UF differ in terms of history, urodynamic results, and magnetic resonance imaging (MRI) findings. The study included women with proven stress urinary incontinence (SUI) based on history (questionnaire, grade II) 12, clinical findings (positive stress test) and urodynamic findings (cystometric exclusion of detrusor hyperactivity in all women) 13. Urethral closure pressure was classified as normal (greater than (100 age) in cmh 2 O), lowered (less than (100 age) to 20 cmh 2 O), or abnormal (less than 20 cmh 2 O). All the women reported spontaneous vaginal deliveries (women with vaginal surgical delivery were excluded). Average parity was 2.0 and 75.8% of the women were primiparae or secundiparae. A history of prior urogynecologic surgery for prolapse or incontinence was a further exclusion criterion. Women who additionally had clinically relevant urogenital prolapse (stage II and higher) were excluded (11 women Aa, Ba = stage 0; 43 women Aa, Ba = stage I) 14. All the study patients underwent introital ultrasonography (vaginal sector scanner, 5-MHz, 90 angle, B-K Medical, Medizinische Geräte GmbH, Berlin, Germany) to assess the mobility of the neck of the bladder. The ultrasound examination was performed with the patient in the halfsitting position. The transducer was placed at the vaginal introitus in the area of the external urethral orifice, applying light pressure (checked on the screen to exclude displacement or compression of the urethra) and aligning the transducer axis to the upright body axis. Settings were adjusted to ensure optimal scan resolution. The bladder filling volume was 300 ml in all patients 15.UF was diagnosed when the proximal urethra opened during straining (Figures 1 and 2). We trained the women to push as hard as possible, but did not simultaneously measure the abdominal pressure. We differentiated funneling of the proximal urethra and opening of the entire urethra during leaking (no woman leaked during a Valsalva maneuver). Displacement of the bladder neck with straining was additionally classified as descent with predominant opening of the urethrovesical angle (increase > 120 in the angle between the urethral axis and bladder floor) or of the inclination angle (increase > 60 in the angle between the body axis and urethral axis). Mixed descent was assumed when both angles showed the respective increase in size. All three types of descent were associated with a decrease in the distance of the bladder neck from the line through the inferior border of the symphysis pubis (perpendicular to the body axis). All the patients underwent MRI as part of their preoperative diagnostic work-up after informed consent had been obtained. MRI was performed with the patient supine and the legs supported in a slightly elevated position. Images were acquired at 1.5 Tesla without the administration of contrast medium using a body phased-array coil (Magnetom Vision, Siemens, Erlangen, Germany). A standardized protocol with the following acquisition parameters was used: proton-density(pd)- weighted turbo spin-echo (TSE) sequences, repetition time (TR) of 2200 ms, echo time (TE) of 15 ms, right left phase encoding, axial slice orientation with a field of view of mm, an image matrix of , a slice thickness of 4 mm and an interslice gap of 0.8 mm (distance factor 0.2). The axial images were analyzed at the level of the bladder neck and at the proximal and middle urethra. Additionally acquired coronal and sagittal MR images were used for confirmation of the findings. Pathomorphologic changes of the urethra, levator ani muscle, and endopelvic fascia were assessed qualitatively because quantitatively determined normal values in healthy nulliparous women show large standard deviations 16, and there are no significant differences between continent and incontinent women 17. MRI findings were considered abnormal when they deviated from the following appearance (Figure 3): Urethra: Depiction of a circular external urethral sphincter muscle of the same signal intensity as that of the obturator internus muscle and round configuration of the urethral lumen. Levator ani muscle: Depiction of the bilateral origin of the levator ani muscle at the pubic bone without discontinuity or complete loss of muscle fibers, same signal intensity as that of the obturator internus. Endopelvic fascia: Lateral: Low-intensity fusion of tissues between the lateral vaginal wall and the levator ani muscle at the level of the urethra, resulting in symphyseal concavity of the anterior vaginal wall. Central: Continuous band-like structure of low signal intensity between the tunica submucosa of the anterior vaginal wall and the external urethral sphincter muscle representing the muscular coat of the vagina. Statistical analysis The data were recorded using Excel 97. Statistical analysis was performed with SPSS 9.0 for Windows (Student s t-test, correlation z-test, Chi-square test for categorial data). The probability of error was α = 0.05, yielding a significance level of P < α. The MR images were assessed a second time by the first author and

3 Urethral funneling in women with stress urinary incontinence 289 Figure 1 Introital ultrasound scan of the true pelvis in a patient with urethral funneling (arrow). Mediosagittal scan showing the inferior border of the symphysis pubis (S), urethra (dotted line), and bladder (B) at rest (a) and during Valsalva maneuver (b). a second investigator without knowledge of the initial interpretation to confirm the reproducibility of the criteria used for evaluation. Methods, definitions, and units conform to the standards recommended by the International Continence Society, except where specifically noted. The MR images were evaluated without knowledge of whether or not UF was present. The study was approved by the university s ethics committee (Charité Hochschulmedizin Berlin). RESULTS In the 54 women (mean age 52 ± 11 years) with SUI, urethral funneling (UF) during straining was present on introital ultrasound examination in 59% (n = 32) (Group 1, Figure 1) and absent in 41% (n = 22) (Group 2, Figure 2). Ultrasonography demonstrated descent with predominant opening of the urethrovesical angle during straining in 43% (n = 23), descent with predominant opening of the inclination angle in 22% (n = 12), Figure 2 Introital ultrasound scan of the true pelvis in a patient without urethral funneling. Mediosagittal scan showing the inferior border of the symphysis pubis (S), urethra (dotted line), and bladder (B) at rest (a) and during Valsalva maneuver (b). and mixed descent in 35% (n = 19). Descent with predominant opening of the urethrovesical angle was more frequently associated with funneling than rotational descent (P = 0.017). The mean age of the women in Group 1 was 53 ± 10 years versus 51 ± 12 years in Group 2 (P = 0.208). The percentages of nulliparous and parous women were 22% and 78% in Group 1 and 54% and 46% in Group2(P = 0.013). The clinical examination revealed no prolapse of the anterior vaginal wall (Aa, Ba = stage 0) in 22% and 18% of the patients in Group 1 and Group 2, respectively, and slight prolapse (Aa, Ba = stage I) in 78% and 82%, respectively (P = 0.741). The urodynamic measurements showed no differences between the patients with UF (Group 1) and without UF (Group 2). Urethral closure pressure at rest was normal (greater than (100 age) in cmh 2 O) in 19% in Group 1 versus 33% in Group 2; lowered (less than (100 age) to

4 290 Tunn et al. Table 1 Incidence of morphologic defects of the urethra, levator ani muscle, and endopelvic fascia detected by magnetic resonance imaging in relation to the demonstration of urethral funneling by introital ultrasonography (no data on fascial morphology: n = 3) MRI appearance Urethral funneling Group 1 (n = 32), % No urethral funneling Group 2 (n = 22), % P Urethral sphincter muscle defects Reduced posterior muscle mass Omega shape Increased signal intensity Levator ani muscle defects Increased signal intensity Complete bilateral absence of origins at pubic bone Loss of substance Endopelvic fascial defects Central defect Lateral defect Loss of concave vaginal configuration Figure 3 Axial proton-density-weighted magnetic resonance image at the level of the proximal urethra showing increased signal intensity of the levator ani muscle (LA) relative to the obturator internus muscle (OI) in a 51-year-old woman with stress urinary incontinence. Omega-shaped dehiscence (dotted line) of the external urethral sphincter muscle in stress urinary incontinence. S, symphysis; V, vagina. 20 cmh 2 O) in 55% versus 43%; and abnormal (less than 20 cmh 2 O) in 26% versus 24% (P = 0.507). Ultrasonographic demonstration of UF was not associated with a significantly higher incidence of morphologic defects of the urethra, levator ani muscle, or endopelvic fascia (Table 1), nor with multiple defects of the stress urinary continence mechanism (P = 0.568). Dynamic assessment of the bladder neck and the presence of UF with straining were compared with the findings of MRI. Neither rotational, vertical, nor mixed descent of the urethra and bladder was found to be associated with a higher incidence of defects of the urethra (P = 0.543), levator ani (P = 0.605), or endopelvic fascia (P = 0.366). DISCUSSION The incidence of 59.3% of urethral funneling in women with stress urinary incontinence found in the present study is within the wide range reported in the literature 3 6,10. The average age of the women with UF was 2 years above that of the women without UF; data in the literature for comparison are not available. The significantly higher parity of the women with funneling identified in our study is not confirmed by results reported in the literature. Rather, most investigators regard the first vaginal delivery as the main factor influencing the structure of the continence mechanism 3,17.Baderet al., investigating women during the first 2 weeks of the postpartal period, found a significant increase in the incidence of ultrasonographically demonstrated UF only with increasing parity 18. Since women with clinically relevant prolapse were not included in our study, the expectation that women with stage 0 or I changes in the area of the anterior vaginal wall do not have a different incidence of UF was confirmed. Sonographic differentiation of downward movement of the bladder neck into descent with predominant opening of the urethrovesical angle (increase > 120 in the angle between the urethral axis and the floor of the bladder), descent with predominant opening of the inclination angle (increase > 60 in the angle between the body axis and the urethral axis), and mixed descent revealed a significantly higher occurrence of UF in combination with descent with predominant opening of the urethrovesical angle. This appears to be a phenomenon that can be explained mechanically in that descent with predominant opening of the inclination angle leads to kinking of the urethra, which may prevent UF, at least during straining. Our results do not confirm any correlation between urodynamic parameters of the urethra (decreased urethral closure pressure or a low-pressure urethra in the pressure profile at rest 19 ), lower leak point pressure 20 and the presence of UF, which clinicians like to establish. This may be due to a lack of power of our study. Funneling of the urethra was not associated with a decreased urethral closure pressure in our study population, possibly because the number of subjects was too small. We did not measure the leak point pressure in our study population. The focus of our study was on the comparison of morphologic abnormalities of the stress urinary

5 Urethral funneling in women with stress urinary incontinence 291 continence mechanism depicted on MR images in stressincontinent women with and without UF. To this end, MRI defects of the urethra, levator ani muscle, and endopelvic fascia were analyzed. An increased signal intensity indicating a reduction of the posterior portion of the striated urethral sphincter muscle was used as an MRI criterion of a morphologic defect of the urethra 21,22. We took this course since continent nulliparous women consistently show a circular configuration of this muscle complex 23 with a signal intensity comparable to that of the obturator internus muscle, which has been proposed to represent the normal MRI appearance 16.Alackof association between morphologic abnormalities of the urethra and UF may be due to a loss of striated muscle fibers in the urethra that occurs with aging 24. The lack of correlation between UF and a loss of substance of the levator ani muscle presenting on MRI as the absence of the origin of this muscle at the pubic bone (i.e. loss of its anterior portion) confirms earlier studies suggesting that this criterion of a levator ani defect does not provide an explanation for the pathogenesis of SUI. These are anatomic variations rather than evidence of morphologic abnormalities resulting from muscular changes 16. A more reliable criterion is the MR signal intensity of the levator ani, which indicates morphologic changes of this muscle based on its chemical composition 17,25 and has been demonstrated by studies comparing the MRI appearance of skeletal muscles with histologic findings 26,27. In our study, women with UF more often had a higher signal intensity of the levator ani muscle (Figure 3). CONCLUSIONS Various studies have shown that MRI is an excellent diagnostic tool for assessing the stress urinary continence mechanism (urethra, levator ani muscle, and endopelvic fascia) in continent nulliparae 16,28 andinwomenwith SUI 17,21. We therefore expected to encounter a higher incidence of morphologic abnormalities of the stress continence mechanism, in particular of the urethra, in women with SUI and UF compared to women without funneling. These expectations were disappointed. The results of our study in a homogeneous population (no women with stage II or greater prolapse, no nulliparae) and the wide variation that exists in reported frequency rates of UF suggest that UF is a typical functional state of the urethra in SUI that results from the multifactorial origin of SUI 29. The relatively low rate of UF of 59.3% in our study may be due to the fact that introital ultrasonography was performed with the patient in the half-sitting position and that no contrast medium was administered. However, even if one assumes that only the more pronounced forms of UF were detected with the examination technique employed in our study, it is noteworthy that not even these more severe forms of funneling were morphologically distinct from the findings in the remainder of the study population. Whether the demonstration of funneling in continent women 30 indicates an intrinsic weakness of the stress urinary continence mechanism or imminent SUI in continent parous women, remains to be determined in further studies. The easy handling of introital ultrasound for assessment of the lower urinary tract and the lack of comparable studies justify further investigation of the examination technique presented here. REFERENCES 1. DeLancey JOL. 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Acta Obstet Gynecol Scand 1952; 31: Abrams P, Cardozo L, Fall M, Griffiths D, Rosier P, Ulmsten U, van Kerrebroeck P, Victor A, Wein A. The standardisation of terminology of lower urinary tract function. Neurourol Urodyn 2002; 21: Bump RC, Mattiasson A, Bo K, Brubaker LP, DeLancey JOL, Klarskov P, Shull BL, Smith ARB. The standardization of terminology of female pelvic organ prolapse and pelvic floor dysfunction. Am J Obstet Gynecol 1996; 175: Schaer GN, Kölbl H, Voigt R, Merz E, Anthuber C, Niemeyer R, Ralph G, Bader W, Fink D, Grischke E, Hanzal E, Koechli OR, Köhler K, Munz E, Perucchini D, Peschers U, Sam C, Schwenke A. Empfehlungen der Arbeitsgemeinschaft Urogynäkologie zur Sonographie des unteren Harntraktes im Rahmen der urogynäkologischen Funktionsdiagnostik. Ultraschall Med 1996; 17: Tunn R, DeLancey JOL, Howard D, Ashton-Miller JA, Quint LE. Anatomic variations in the levator ani muscle, endopelvic fascia, and urethra in nulliparas evaluated by magnetic resonance imaging. 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6 292 Tunn et al. 17. Tunn R, Paris S, Fischer W, Hamm B, Kuchinke J. Static magnetic resonance imaging of the pelvic floor muscle morphology in women with stress urinary incontinence and pelvic prolapse. Neurourol Urodyn 1998; 17: Bader W, Kauffels W, Degenhardt F, Schneider J. Postpartale Sonomorphologie des Beckenbodens. Geburtsh Frauenheilk 1995; 55: Dietz HP, Clarke B. The urethral pressure profile and ultrasound imaging of the lower urinary tract. Int Urogynecol J 2001; 12: Huang WC, Yang JM. Bladder neck funneling on ultrasound cystourethrography in primary stress urinary incontinence: a sign associated with urethral hypermobility and intrinsic sphincter deficiency. Urology 2003; 61: Klutke CG, Golomb J, Barbaric Z, Raz S. The anatomy of stress incontinence: Magnetic resonance imaging of the female bladder neck and urethra. JUrol1990; 143: Klutke CG, Raz S. Magnetic resonance imaging in female stress incontinence. Int Urogynecol J 1991; 2: Strohbehn K, Quint LE, Prince MR, Wojno KJ, DeLancey JOL. Magnetic resonance imaging anatomy of the female urethra: A direct histologic comparison. Obstet Gynecol 1996; 88: Perucchini D, DeLancey JOL, Ashton-Miller JA, Galecki A, Schaer GN. Age effects on urethral striated muscle. II. Anatomic location of muscle loss. Am J Obstet Gynecol 2002; 186: Tunn R, DeLancey JOL, Howard D, Thorp JM, Ashton- Miller JA, Quint LE. MR imaging of levator ani muscle recovery following vaginal delivery. Int Urogynecol J 1999; 10: Schedel H, Reimers CD, Vogl T, Witt TN. Muscle edema in MR imaging of neuromuscular diseases. Acta Radiol 1995; 36: Fleckenstein JL, Watumull D, Conner KE. Denervated human skeletal muscle: MR imaging evaluation. Radiology 1993; 187: Tan IL, Stoker J, Zwamborn AW, Entius KAC, Calame JJ, Laméris JS. Female pelvic floor: Endovaginal MR imaging of normal anatomy. Radiology 1998; 206: Petri E, Koelbl H, Schaer G. What is the place of ultrasound in urogynecology? A written pannel. Int Urogynecol J 1999; 10: Bergman A, McKenzie C, Ballard CA, Richmond J. Role of cystourethrography in the preoperative evaluation of stress urinary incontinence in women. J Reprod Med 1988; 33:

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