Neurourology and Urodynamics 22:269^276 (2003)
Compliance of the Bladder Neck Supporting Structures: Importance of Activity Pattern of Levator Ani Muscle and Content of Elastic Fibers of Endopelvic Fascia Matija Barbic› ,1* Boz›o Kralj,2 and Andrej C˛r3
1
Department of Obstetrics and Gynecology, University Medical Center Ljubljana, Slovenia 2 University College of Health Sciences, University of Ljubljana, Slovenia 3 Institute for Histology and Embryology, Medical Faculty, University of Ljubljana, Slovenia Aims: Firm bladder neck support during cough, suggested to be needed for e¡ective abdominal pressure transmission to the urethra, might depend on activity of the levator ani muscle and elasticity of endopelvic fascia. Methods: The study group of 32 patients with stress urinary incontinence and hypermobile bladder neck, but without genitourinary prolapse, were compared with the control group of 28 continent women with stable bladder neck. The height of the bladder neck (HBN) and compliance of the bladder neck support (C) were assessed, the latter by the quotient of the bladder neck mobility during cough and the change in abdominal pressure. By using wire electrodes, the integrated full-wave recti¢ed electromyographic (EMGave) signal of the levator ani muscle was recorded simultaneously with urethral and bladder pressures. The pressure transmission ratio (PTR), time interval between the onset of muscle activation and bladder pressure increment (DT), and area under the EMGave curve during cough (EMGcough) were calculated. From bioptic samples of endopelvic fascia connecting the vaginal wall and levator ani muscle, elastic ¢ber content was assessed by point counting method. Mann-Whitney test was used to compare all the variables. Correlations between the parameters were evaluated by using the Spearman correlation coe⁄cient. Results: In the study group, HBN was signi¢cantly lower (P < 0.001), C was signi¢cantly greater (P < 0.001), and PTR was signi¢cantly lower (P < 0.001). In the study group, the muscular activation started later (median, DTl, 0.147 second; DTr, 0.150 second), and in the control group, it preceded (DTl, 0.025 second; P < 0.001; DTr, 0.050 second; P < 0.001) the bladder pressure increment. EMGcough on the left side was signi¢cantly greater in the study group (P < 0.046). Elastic ¢ber content showed no di¡erence between the groups. The analysis of all patients revealed negative correlations between C and PTR (r ¼ 0.546; P < 0.001) and between C and DTl (r ¼ 0.316; P < 0.018). Conclusions: Firm bladder neck support enables e¡ective pressure transmission. Timely activation of the levator ani seems to be an important feature. Neurourol. Urodynam. 22:269 ^276, 2003. ß 2003 Wiley-Liss, Inc. Key words: bladder neck support; elastic ¢bers; endopelvic fascia; levator ani muscle; stress urinary incontinence
INTRODUCTION
One of the causes of stress urinary incontinence (SUI) is very likely the ine⁄cient transmission of elevated intraabdominal pressure to the urethra [Enh˛rning, 1961]. A stable position of the anterior vaginal wall, on which the urethra and bladder base are lying, is suggested to be crucial in e¡ective compression of urethral lumen by downward force of abdominal pressure [DeLancey, 1994]. An unstable position of the anterior vaginal wall, which can be observed as hypermobility of the bladder neck during elevated intra-abdominal pressure [Hodgkinson et al., 1958; Green, 1962; Crystle et al., 1971; Blaivas and Fisher, 1981; Kohorn et al., 1986; K˛lbl et al., 1988; Schaer et al., 1995] might be the consequence of greater compliance of supporting structures [DeLancey, 1994], i.e., the endopelvic fascia and levator ani muscle, to which endopelvic ß 2003 Wiley-Liss, Inc.
fascia connects the anterior vaginal wall [DeLancey and Starr, 1990]. The aim of this study was to ¢nd the relevance of the activity of the levator ani muscle and of the content of elastic ¢bers of endopelvic fascia for the support of the bladder neck during cough.Therefore, we studied the kinesiologic properties of the levator ani muscle, relative content of elastic ¢bers in endopelvic fascia tissues, and compliance of the bladder neck during
*Correspondence to: Matija Barbic› , M.D., M/Sc., Department of Obstetrics and Gynecology, University Medical Center Ljubljana, S lajmerjeva 3, SI-1000 Ljubljana, Slovenia. E-mail: matija.barbic@guest.arnes.si Received for publication 23 May 2002; Accepted 2 December 2002 Published online inWiley InterScience (www.interscience.wiley.com) DOI 10.1002/nau.10116
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cough in a group of women with SUI associated with hypermobility of the bladder neck, and in the control group of women free of these signs. MATERIALS AND METHODS
In the study, 60 patients were enrolled between February of 1998 and May of 2001. The study group was represented by 32 parous women (31had 2, and 1had 3 vaginal deliveries) with clinically (examination þ orientation perineal ultrasound) con¢rmed hypermobility of the anterior vaginal wall (without uterovaginal descent) and stress urinary incontinence diagnosed according to the International Continence Society (ICS) standards; they had been planned for Burch colposuspension [Burch, 1961]. The study group women were compared with the control group of 28 parous women (26 had 2, and 2 had 1 vaginal delivery) with clinically stable anterior vaginal wall (mobility of the bladder neck less than 1 cm on perineal ultrasound), and urinary incontinence excluded by the 1-hour pad test (ICS); they had been planned for operation of myomatous uterus by means of laparotomy. The size of the myomas did not exceed 10 cm in diameter. The mean patient age was 43.03 years (range, 27^52 years) in the study group, and 43.92 years (range, 30 ^52 years) in the control group. None of the women had previous operations. All had regular menstrual cycles. Informed consent was obtained from all participating women. The study had been approved by the National Ethics Committee. The methods, de¢nitions, and units used conform to the standards recommended by the ICS, except where speci¢cally noted. Before the operations, all the women had electromyographic (EMG) measurements recorded, combined with intravesical and urethral pressure measurements, which was followed by perineal ultrasound measurements combined with abdominal pressure measured in the rectum. During the measurements, the patients were in the semilithotomy position. Dantec Menuet Urodynamic Investigation System with the Menuet System Software version 4.00 was used for EMG signal and pressure recordings. For the recordings, we used a standard setting cystometry (‘‘timebase’’ 5 seconds) with three pressure channels and one EMG channel. The EMG signal was processed by a full-wave recti¢er followed by a lowpass R ¢lter, producing an average EMG signal (EMGave ( j EMG j dt)). To prepare the patient for the measurements, two thin isolated wires [Vereecken and Verduyn, 1970] (manufactured by ‘‘Pinki’’, Ljubljana, Slovenia, 15 cm, 260 O/m, enamel for isolation), which had had the insulation removed at the tip for a distance of 2 mm, and had been connected at a constant distance, were inserted through the vagina (by means of a 2.5-cm-long 24-gauge steel needle), which was removed immediately) in the left and right side of the levator ani muscle under transvaginal digital control, cephalad to caruncles. The quality of the signals from either side of the muscle was
assessed both visually on the screen and by means of the loudspeaker. If necessary, minor corrections of the electrode positions were achieved by gently pulling the wires. For urethral and intravesical pressures, an 8-French double microtip transducer catheter with lumen, model 22K 62, was used, and for abdominal pressure, measured in the rectum, the external transducer 22K11 Statham, connected to the balloon catheter 21P110 by infusion system was used (all accessories, Dantec, Denmark). A urethral catheter was installed in the urethra with the distal sensor positioned in the bladder and the proximal sensor in the proximal urethra. Both sensors were oriented at 3 o’clock. In the ¢rst step, cystometry was performed with warm saline solution at the bladder volume of up to 250 mL, at a rate of 50 mL/min and disconnected wire electrodes. Then, we reconnected the wire electrodes of the right side of the muscle and asked the patient to cough to test the quality of the signal again. After a few minutes of complete relaxation, the recordings were performed, during which time the patient had to cough three times (Fig. 1). The procedure was repeated at the left side of the muscle. We then pulled the urethral catheter out and performed perineal ultrasound measurements (Toshiba SSA-250A; semiconvex abdominal probe PVT-375MT) of the height of the bladder neck and its mobility during cough [Schaer et al., 1995; Barbic› and Kralj, 2000] simultaneously with rectal pressure measurements. The ultrasound probe was placed against the vulva in the sagittal plane to obtain views of the bladder, bladder neck, urethra, and symphysis. Caution was taken not to disturb the position of the bladder neck. The patient was asked to cough. With the command ‘‘playback’’, the last 2 seconds of the event were recorded. In the ultrasound image of the bladder neck
Fig. 1. Urodynamic and integrated full-wave rectified electromyographic (EMGave) signal traces: 1, detrusor pressure; 2, bladder pressure; 3, abdominal pressure; 4, EMGave; 5, urethral pressure.
Bladder Neck Supporting Structures
position at rest, we drew the central line of the symphysis [Schaer et al., 1995]. From the inferior point of this line, we drew a line parallel with the inferior border of the screen, which represented the imaginary pelvic £oor level, and determined the angle between both lines. Bladder neck position was determined at the junction of the bladder neck and posterior urethral wall. We then repeated the described steps in the image representing the bladder neck in lowermost position considering that the angle between the central line of the symphysis and the determined pelvic £oor had to be the same (Fig. 2A,B). Both images were then printed on Polaroid ¢lm.
Fig. 2. Polaroid prints of perineal ultrasound measurement of bladder neck positions. A: Bladder neck position at rest. C.L., central line of the symphysis; P.F.L., imaginary pelvic floor level. The angle between both lines is 135 degrees. B: Bladder neck in the lowermost position during cough. The difference in bladder neck position compared with position at rest was 4.6 mm, representing mobility of the bladder neck during cough.
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From the screen and Polaroid prints, we calculated and determined the variables, listed below. The calculations were made by two investigators who were blinded to the patients’ continent status. All the measurements were mean values of two or three consecutive events. PTR: Pressure transmission ratio ¼ (D urethral pressure/D bladder pressure) 100. DT: Time interval between the onset of muscle activity during cough and onset of bladder pressure increment during cough. The basal value of EMGave oscillated continuously; however, at the beginning of activity, the trace was continuously rising, without oscillation to the basal line. The onset of muscle activity during cough was considered to be at the point from which, for at least three consecutive movements of the cursor, a continuous rise of EMGave trace was observed, without any de£ection to the basal line; the onset of bladder pressure increment was determined in the same way, i.e., at the point where the pressure increased for at least 1 cm H2O, and raised continuously (Fig. 3). If the onset of the bladder pressure increment preceded the onset of muscle activity, the value was negative. The value was expressed in seconds. The measurements were done separately for the left and the right side of the muscle. EMGcough: Activation of the levator ani muscle during cough ¼ the area under the EMGave curve during cough. The value was expressed in microvolt seconds. The measurements were done separately for the left and the right side of the muscle. HBN: The height of the bladder neck ¼ the perpendicular distance between the bladder neck and imaginary pelvic £oor line measured at rest (Fig. 2A).
Fig. 3. Determination of the time interval between the onset of muscle activity during cough and the onset of bladder pressure increment during cough ( T). EMGave, integrated full-wave rectified electromyographic signal.
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C: Compliance (C) of the supporting structures ¼ a quotient between the bladder neck mobility during cough and the rectal pressure during cough (bladder neck mobility/D rectal pressure). Mobility of the bladder neck was determined as the di¡erence in the bladder neck position (according to imaginary pelvic £oor level) in resting and lowermost positions (Fig. 2A,B). The value was expressed in mm/cm H2O. Tissue Sampling
During the operation, the Retzius space was prepared and a bioptic sample of the tissue connecting the lateral vaginal wall and the levator ani muscle at the level of the bladder neck was taken. The level of the bladder neck was determined according to the position of the Foley catheter balloon. The specimen was immediately ¢xed in 10% formalin and embedded in formalin according to routine procedures. Elastic ¢ber content was analyzed in histologic sections stained according to Weigert van Gieson method. Areal density was determined with a point counting technique by a person who was blinded to the clinical history of the patients [Howard and Reed, 1998]. Mann-Whitney test was used to compare all the variables between the groups. Correlations between the parameters were evaluated with Spearman coe⁄cients.
In one patient, bioptic sampling of the tissue was followed by bleeding of approximately 1,000 mL, and a blood transfusion was needed. Three bioptic samples were unusable for histologic evaluation of elastic ¢ber content because of tissue damage that occurred during histological preparation. Basic descriptive statistics (median values, quartile ranges) and P values are presented inTable I. In the study group, C was signi¢cantly greater and HBN and the PTR were signi¢cantly lower than in the control group. Median DT for the left and the right side of the muscle were negative in the study group, representing mostly a delayed onset of muscle activity regarding the onset of bladder pressure increment. In the control group, these values were positive, suggesting mostly an early onset of muscle activity. EMGcough left was signi¢cantly greater in the study group. Light microscope examination of the slides, stained according to Weigert van Gieson, showed that elastic ¢bers in the endopelvic fascia were sparse. They were very ¢ne, displaying longitudinal orientation. Individual elastic ¢bers were tightly coiled and rippled in appearance (Fig. 4). Areal density showed no di¡erences between the groups. Taking all the patients into consideration, we found negative correlations between C and PTR (r ¼ 0.546; P < 0.001) (Fig. 5) and between C and DT left (r ¼ 0.316; P < 0.018) (Fig. 6). DISCUSSION
RESULTS
Insertion of wire electrodes on the left side of the levator ani muscle in two patients and on the right side of the levator ani muscle in three patients failed, despite repeated attempts. Having had technical problems with the double microtip transducer catheter, we failed to measure and calculate the PTR in three patients, whereas in two patients the extremely high values were very likely the artifacts due to direct pressure of the surrounding urethral tissue on catheter sensors. A technical problem with the Statham transducer was the reason for not being able to measure the abdominal pressure in one patient.
The structures, mostly involved in the bladder neck support are the levator ani muscle and endopelvic fascia. According to the ‘‘hammock’’ hypothesis, the importance of bladder neck support, at the level of which the urethral lumen should not be encircled by sphinteric muscle [Gosling, 1979], would be in providing a ¢rm layer to which intra-abdominal forces should compress the urethral lumen [DeLancey, 1994]. When the supporting structures are compliant, the result could be expressed as ine⁄cient pressure transmission as well as hypermobility of the bladder neck. Mobility of the bladder neck can be observed by many methods [Hodgkinson et al., 1958; Green, 1962; Crystle et al.,
TABLE I. C, HBN, PTR, and EMG Parameters and Elastic Fiber Content in the Study and in the Control Group Study group
C (mm/cm H2O) HBN (mm) PTR DT left (s) DT right (s) EMGcough left (mVs) EMGcough right (mVs) Elastic %
Median
25/75 Percentile
0.081 19.900 75.5 0.147 0.150 385 260 4.30
0.064/0.105 12.8/24.3 68.0/92.5 0.300/0.000 0.360/0.000 181/609 143/511 2.00/6.50
Control group Median 0.050 24.350 107.0 0.025 0.050 239 291 4.00
25/75 Percentile 0.031/0.073 15.9/29.2 87.0/137.0 0.000/0.106 0.000/0.126 122/348 141/697 2.60/6.40
P value <0.001 <0.001 <0.001 <0.001 <0.001 <0.046 <0.591 <0.635
C, compliance; HBN, height of the bladder neck; PTR, pressure transmission ratio; DT, time interval; EMG, electromyographic.
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Fig. 4. Elastic fibers in endopelvic fascia tissue. The point counting grid is visible.
1971; Blaivas and Fisher, 1981; Kohorn et al., 1986; K˛lbl et al., 1988; Schaer et al., 1995]. By themselves, they do not reveal the extent of compliance of supportive structures, because mobility of the bladder neck during cough is the product of supportive tissues compliance as well as of intra-abdominal pressure forces. Therefore, to evaluate the compliance of supportive tissues, we used the coe⁄cient between the bladder neck mobility during cough and changes in intra-abdominal pressure. This relationship is an inverted evaluation to ‘‘sti¡ness’’ of the bladder neck support previously described [Howard et al., 2000]. Perineal ultrasound, the method that seems to be least invasive and most reproducible, was used for this purpose [Schaer et al., 1995; Barbic› and Kralj, 2000]. To con¢rm that there were no clinically signi¢cant di¡erences in the position of anterior vaginal wall at the level of the bladder neck, we also determined the position of the bladder neck. Despite signi¢cant di¡erences in the bladder neck position between the groups, the di¡erences were within the
Fig. 5. Correlation between compliance and pressure transmission ratio (PTR).
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Fig. 6. Correlation between time interval between the onset of muscle activity during cough and the onset of bladder pressure increment during cough ( T) left and compliance.
range of only a few millimeters, which, according to ICS recommendations, could be disregarded [Bump et al., 1996]. Despite the possibility that clinically hypermobile bladder neck could only be the consequence of a higher intra-abdominal pressure during cough, statistical analysis revealed significantly greater compliance (C) in the study group, with minimal overlapping of the results, which is in agreement with the ¢ndings by Howard et al., who found a weaker sti¡ness of bladder neck support in SUI patients [Howard et al., 2000]. This ¢nding additionally was con¢rmed by the comparison of PTR between the groups. Namely, the compliant bladder neck support fails to enable e¡ective compression of the urethra by downward forces, which would be expressed by lower PTR values in a¡ected patients [DeLancey, 1994]. In the study group, the median PTR of approximately 75%, measured at the level of the bladder neck, revealed insu⁄cient pressure transmission. However, the median PTR of approximately 107% in the control group suggested that, in some patients, the pressure transmission was more than perfect.These higher values were partly due to the position of the urethral sensor in the ¢rst 30% of the urethral lumen, where the in£uence of muscular contraction on intraluminal urethral pressure is low, although not completely absent, and to ‘‘not yet’’ perfect measurement techniques [Abrams et al., 1988], which was very likely re£ected in two extremely high PTR values. However, the median PTR values suggest that, in the study group, the suburethral layer was less ¢rm than in the control group. Considering these facts, and also the negative correlation between C and PTR, suggesting that stable bladder neck support enables higher PTR, we agree that ¢rm suburethral support is important and that the hammock hypothesis could be accepted as valid. It has been found that women with stress urinary incontinence and uterovaginal descent have a signi¢cant increase in denervation of the levator ani muscles [Gilpin et al., 1989;
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Smith et al., 1989]. However, the denervation/reinnervation process does not necessarily lead to an a¡ected muscular function [Podnar et al., 2000; Vodus› ek, 2000], yet it is important that, in women with stress urinary incontinence, a di¡erent ‘‘behavior’’ of the levator ani muscle has been found [Deindl et al., 1994]. To ¢nd the manner in which the levator ani muscle during cough behaves, kinesiologic EMG [Vodus› ek, 1994] using wire electrodes [Vereecken and Verduyn, 1970] was applied in our study. The comparison of DT between the two groups revealed a predominantly early activation on both sides of the levator ani muscle in the control group, and a predominantly late activation on both sides of the levator ani muscle in the study group. In previous studies, it has been found that, in healthy women, the pressure increment in mid and distal urethra during a stress episode precedes the bladder pressure increment by 0.100 to 0.200 second because of a contraction of the urethral and periurethral muscles [Constantinou and Govan, 1982; Kooi et al., 1984; Thind et al., 1991]. Because these muscles, as well as most of the levator ani muscle, are innervated by terminal branches of the pudendal nerve [Percy and Parks, 1981] and are activated during cough [Bhatia and Rosenzweig, 1991], we expected the same time interval. However, in the control group, the median DT revealed that the levator ani muscle contraction preceded the bladder pressure increment by 0.025 second on the left, and by 0.050 second on the right side. In the study group, DT was negative: the levator ani muscle contraction started later ( 0.147 second on the left side, 0.150 second on the right side) than the bladder pressure increment. In comparison with previous data, our results show that, in the control group, the interval was approximately by 10-times shorter, and in the study group approximately 10-times longer. This ¢nding could be the bias due to technical characteristics of EMGave traces. However, the DT di¡erences between the study and the control group were in the range of previous reports [Thind et al., 1991]. Looking for the reason of the negative values of DT in the study group, we may only suggest a noncoordinated contraction of involved muscular groups, i.e., abdominal and pelvic musculature. Knowing that, in SUI patients, the prolonged conduction in pudendal perineal branches, innervating the levator ani muscle, is in range of a few microseconds [Snooks and Swash, 1984], we can hardly consider this ¢nding to be the reason for late contraction of the levator ani muscle. Although we were not in the position to simultaneously measure the EMG signal from the left and right side of the levator ani muscle, some asymmetry between the measurements on the right and the left side was observed, i.e., the values on the left and right side were never ‘‘mirror’’ images. Although the integral of full-wave recti¢ed electromyographic record is proportional to the force generated by the muscle [Milner-Brown and Stein, 1975], a nonstandardized interelectrode distance, di¡erent measurement sites and position of the electrodes in relation to the muscle ¢bers orientation may
account for variability in EMG recorded muscular activity [Brown, 1984]. We used the standard interelectrode distance and measurement sites. However, after insertion of the electrodes in the muscle, the interelectrode distance and its position in relation to the muscle ¢ber orientation could not be further controlled, which could contribute to the observed differences. These facts should also be considered regarding great variability of the results, observed also in a previous study, in which wire electrodes had been used but the measured amplitudes were not assessed in terms of absolute values [Deindl et al., 1994]. Because in our study a greater number of patients were included, we also evaluated the electrical muscular activity in terms of absolute values, measuring the area under the EMGcough trace: the evaluation was based on comparison of median values between the groups. Surprisingly, in the study group, higher values of EMGcough were found, although in the left side of the levator ani muscle only. The result suggests a stronger activation of the levator ani muscle in patients with hypermobile bladder neck. This explanation would be acceptable, if di¡erences in elastic ¢ber content of endopelvic fascia were proved. However, as discussed further on, this ¢nding was not the case.Therefore, the only explanation for this result is that muscular activation was not a¡ected in cases of minor disturbances of pelvic £oor anatomy, i.e., hypermobility of the bladder neck. We presume that the result was accidental. Endopelvic fascia contains collagen and smooth muscle ¢bers, as well as higher concentrations of elastin ¢bers than is present in the surrounding tissues [DeLancey and Starr, 1990]. It has been known from previous studies that connective tissue’s content of collagen and its subtypes could be di¡erent in SUI patients [Ulmsten et al., 1987; Versi et al., 1988; Bergman et al., 1994; Falconer et al., 1994, 1998; Kean et al., 1997]. However, when hypermobile bladder neck (without uterovaginal descent) is observed, greater compliance of supportive structures could be the consequence of greater elasticity of endopelvic fascia, the feature mainly attributed to elastic ¢ber content [Dass et al., 1999]. For this reason, we studied the elastic ¢ber content of the tissue, connecting the vaginal wall and the levator ani muscle, which we presumed to be part of the endopelvic fascia. However, comparing the percentage of the whole crosssectional areas by elastic ¢bers in the study and control group, we did not ¢nd statistical di¡erences. The elastic ¢bers areal density was in the range predicted for soft tissues [Thompson, 1995]. The result suggests that, even if the biophysical properties of endopelvic fascia in patients with hypermobile bladder neck are di¡erent, these di¡erences can hardly be attributed to di¡erent elastic ¢bers content. On the basis of our results of EMG parameters of the levator ani muscle and elastic ¢ber content of endopelvic fascia, it seems most probable that only the time interval between the onset of muscular activation during cough and the onset of abdominal pressure increment play a role in the bladder neck support compliance. This observation was con¢rmed by a
Bladder Neck Supporting Structures
negative correlation between C and DT left. This ¢nding suggests that the greater the delay in muscular activation, the greater the compliance of bladder neck support. Although the correlation at the right side was not found, an early onset of activation was registered on both sides of levator ani in the control group (regarding intraabdominal pressure); this ¢nding suggests a possible pretension of endopelvic fascia and vaginal wall tissues, which could change their elastic properties. CONCLUSIONS
It seems that an important aspect of stable bladder neck support is the timely activation of the levator ani muscle. The activation, which precedes the contraction of other muscles involved in the cough re£ex, might enable a pretension of endopelvic fascia tissue, which becomes less compliant for stretching by downward forces of increased abdominal pressure. If, in patients with hypermobility, di¡erent biophysical properties of endopelvic fascia of the bladder neck exist, these cannot be attributed to di¡erent elastic ¢ber content. Further studies of the contents of di¡erent collagen types would be needed. ACKNOWLEDGMENTS
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