TY - JOUR
AU - Allen-Mersh, T G
AB - Abstract Background The late onset of pelvic visceral prolapse and incontinence after childbirth injury could be explained by menopause-associated connective tissue weakening. Uterosacral ligament resilience (UsR) was assessed to determine whether it influenced uterine or pelvic floor mobility, or varied with age, vaginal delivery, menopause or histological variations in the ligament. Methods UsR was measured by tensiometry in ligaments from 85 hysterectomy specimens, and was correlated with the presence of symptomatic uterocervical prolapse, prehysterectomy uterine and anorectal mobility, patient age, history of vaginal delivery and menopause. Forty-five of these ligaments were examined for ligament thickness, muscle to collagen ratio, and oestrogen and progesterone receptor density. The results were correlated with UsR. Results UsR was significantly reduced (P = 0·02) in symptomatic uterovaginal prolapse, but there was no correlation with either uterocervical or anorectal descent in women without symptomatic prolapse. There was a significant decrease in UsR with vaginal delivery (P = 0·003), menopause (P = 0·009) and older age (P = 0·005). The uterosacral ligament was significantly thinner and contained fewer oestrogen and progesterone receptors after menopause, but this did not affect UsR. Conclusion Where pelvic floor muscles are weakened, decreases in pelvic connective tissue resilience related to the menopause may facilitate progression to symptomatic pelvic visceral prolapse. Introduction Pelvic floor laxity leads to incontinence or visceral prolapse in 20 per cent of gravid women aged over 50 years1. The most important causes of pelvic floor laxity are muscle injury2 and denervation3 at vaginal delivery. Precautions in obstetric management4–7 can reduce childbirth-related pelvic floor damage, but the increased risks associated with factors such as nulliparity, Asian race, fetal occiput posterior position and high fetal birthweight5 can be avoided only by an unacceptable frequency of elective caesarean delivery2,8. As the symptoms of pelvic floor laxity usually develop three or four decades after childbirth2,9 an improved understanding of the natural history of pelvic floor laxity might allow management that reduced progression to the development of symptoms. The pelvic connective tissues are organized into a fascial sheet that overlies the pelvic floor muscles, and condenses to form ligaments within looser areolar tissues10,11. As primate stature became more upright during evolution, attachment of this fascia to the pelvic sidewalls increased12,13, suggesting that connective tissue plays an increasing role in pelvic visceral stabilization with upright posture14,15. One explanation for the delayed onset of symptoms after childbirth injury could be progressive pelvic floor weakening16 resulting from connective tissue degradation17,18. The resilience of pelvic connective tissue might be affected by at least two factors. First, repair of connective tissue that has been damaged by vaginal delivery involves a change from type I to the weaker type III collagen19. Second, the collagen content of cutaneous connective tissue decreases in women after menopause20, and similar postmenopausal decreases in pelvic connective tissue21–23 might reduce resilience. This study was designed to assess whether variation in pelvic connective tissue resilience correlated with pelvic visceral movement, or was influenced by vaginal delivery, menopause, or changes in collagen or oestrogen and progesterone receptor density. The uterosacral ligament, which is composed of connective tissue, smooth muscle, blood vessels and nerves24, was studied. It arises from the posterolateral aspect of the cervix and runs posteriorly to attach into the presacral fascia at the lower end of the sacroiliac joint25. Uterosacral ligaments were obtained from hysterectomy specimens, and uterosacral ligament resilience (UsR), ligament thickness, muscle to collagen ratio, and oestrogen and progesterone receptor density were measured. The relationships of UsR with pelvic floor mobility, patient age, history of vaginal delivery and menopause, and ligament histology were then determined. Patients and methods Patients Women undergoing abdominal hysterectomy for benign disorders (Table 1) were studied. A note was made of patient age, obstetric history, menopausal status and indication for hysterectomy. Women taking hormone replacement therapy (HRT) were excluded from the study. Women were regarded as having had a vaginal delivery when delivery of a live or stillborn child had occurred via the vagina after 28 weeks of gestation26. Menopause was defined as amenorrhoea of more than 1 year's duration27. All patients gave informed consent to be included in the study, which was approved by the Chelsea and Westminster Hospital Ethics Committee. Table 1 Indications for hysterectomy by age, in the patients studied Indication for hysterectomy . Age ≤ 50 years (n = 41) . Age > 50 years (n = 44) . Menorrhagia 17 13 Fibroids 15 16 Prolapse  1  3 Other bleeding  8 12 Indication for hysterectomy . Age ≤ 50 years (n = 41) . Age > 50 years (n = 44) . Menorrhagia 17 13 Fibroids 15 16 Prolapse  1  3 Other bleeding  8 12 There were no significant differences between age groups. Open in new tab Table 1 Indications for hysterectomy by age, in the patients studied Indication for hysterectomy . Age ≤ 50 years (n = 41) . Age > 50 years (n = 44) . Menorrhagia 17 13 Fibroids 15 16 Prolapse  1  3 Other bleeding  8 12 Indication for hysterectomy . Age ≤ 50 years (n = 41) . Age > 50 years (n = 44) . Menorrhagia 17 13 Fibroids 15 16 Prolapse  1  3 Other bleeding  8 12 There were no significant differences between age groups. Open in new tab Pelvic visceral movement Patients underwent magnetic resonance imaging (MRI) on the day before hysterectomy. The patient was placed in the supine position and 12-Fr Foley catheters (BARD™, Crawley, UK) were placed into the lower rectum and vagina to aid image interpretation. The scanning technique has been described previously28. Correlation of anorectal descent and change in anorectal angle with straining between supine MRI and seated evacuation proctography has been demonstrated29. Imaging was performed at 1·0 tesla on a Magnetom Impact Expert® machine (Siemens, Munich, Germany) with the patient at rest and straining. Pelvic floor descent was achieved by instructing the patients to strain down ‘as if evacuating the bowel or having a baby’. The uterocervical junction was first identified on midline sagittal images, and its change in position between rest and straining was then measured. The descent of the anorectal junction with straining was assessed similarly. Measurement was by a single experienced radiologist using a Sienet Magicview® 1000 computer workstation (Siemens, Munich, Germany). Electronic callipers contained within the workstation software were used to make the measurements. The radiologist was not aware of patient details. Uterosacral ligament and anterior rectus abdominis sheath biopsy Abdominal hysterectomy was performed according to the surgeon's usual technique. After completion of the hysterectomy, either the right or both uterosacral ligaments were removed from the uterus, commencing at the point of insertion of the ligament on to the posterolateral aspect of the uterus at the uterocervical junction and extending for a distance of at least 25 mm. Before resilience measurement, a 10-mm length of the ligament that was perpendicular to its cross-section was taken from the ligament specimen for histological examination. This 10-mm portion was fixed in 10 per cent neutral buffered formalin, and the remaining 15 mm of the ligament specimen was used for resilience measurement. A 15 × 15 mm biopsy of anterior rectus abdominis sheath was removed from the upper edge of the transverse operative incision. Measurement of uterosacral and anterior rectus abdominis resilience Specimens were trimmed to 10 × 10 mm for resilience measurement. Resilience was measured by tensiometry as described previously30–32, using an Instron Series IX Universal Testing Machine (Instron® 5564; Instron, Maidenhead, UK). Resilience is a measure of work where: Work (joules) = Load (newtons) × Tissue extension (centimetres). A load of 1 kN was applied to the specimen at a strain rate of 10 mm/min. The typical relationship of load to extension for a uterosacral ligament is shown in Fig. 1. The straight-line component to the inflection point (x) represents elastic behaviour by the ligament. This is the limit at which the ligament displays elastic properties and is called the plastic limit. Beyond this point any further extension would result in permanent deformity. Resilience describes the work done by the ligament in absorbing the force applied to stretch it to the plastic limit. This value was derived from the area under the curve (A) up to the plastic limit using customized software within the tensiometer. Fig. 1 Open in new tabDownload slide Uterosacral ligament load–extension curve. Ligament resilience describes the work done (joules) by the ligament in absorbing the force applied to stretch it to the plastic limit. This was derived from the area under the curve (A) up to the plastic limit (x) Histological examination Formalin-fixed uterosacral ligament tissue was embedded in paraffin wax with a transverse orientation, so that histological sections demonstrated the ligament cross-section. To determine the relative proportions of collagen and smooth muscle, specimens were stained by the Van Gieson technique33. Oestrogen receptors and progesterone receptors were identified by standard immunohistochemical techniques34. For immunohistochemical studies, breast cancer samples were used as positive controls and mouse ascitic fluid as negative controls. Sections were examined through a light microscope at × 40 magnification with a 25-point Chalkley eye-piece graticule (Pyser-SGI, Edenbridge, UK). Four fields were counted to give a maximum score of 100 graticule points. Relative percentage scores were estimated by means of a previously validated counting technique35–37. For collagen : muscle assessments, the muscle was always assessed as the background substance and when graticule points totally or partially covered collagen this was counted as a ‘hit’. Similarly, when estimating oestrogen and progesterone receptor density, if a graticule point partially or totally covered a receptor this was counted as a ‘hit’. Uterosacral ligament cross-sectional thickness (at right angles to the longitudinal axis of the ligament) was measured using a millimetre-graded magnifying ruler, after Van Gieson staining. Thickness measurements were taken across the midpoint of the cross-section, and across two points situated at a distance of 5 mm laterally in each direction along the longest axis, from the cross-section midpoint. The mean of the three measurements was taken as the ligament thickness. Histological assessments and ligament thickness measurements were made without knowledge of patient details. Statistical analysis Analysis of differences between groups was by Mann–Whitney U and χ2 tests. Correlation was by Pearson test, and regression analysis was performed using the general linear model. Results Patients UsR was measured in the right uterosacral ligaments from 85 women (median age 48 (interquartile range (i.q.r.) 43–64) years). Subgroups were also examined for UsR in the left uterosacral ligament (the first consecutive 12 women), anterior rectus abdominis sheath resilience (the last consecutive 35 women) and for pelvic visceral descent with straining before hysterectomy (22 women without symptomatic uterovaginal prolapse, according to availability). Uterosacral ligaments from the last 45 women were studied histologically. There was a history of vaginal delivery in 59 women (one delivery, 31 women; two deliveries, 17; three or more deliveries, 11), and menopause in 43 women. Four women were undergoing hysterectomy for symptomatic uterovaginal prolapse. There were no significant differences in indications for hysterectomy in women aged over 50 years compared with younger women (Table 1). Uterosacral ligament resilience The median (i.q.r.) right UsR for all 85 women was 0·022 (0·010–0·036) J. In women in whom both ligaments were studied there was no significant difference in left (0·014 (0·007–0·038) J) compared with right (0·017 (0·006–0·040) J) UsR (P = 0·53, n = 12). UsR in the four women who underwent hysterectomy for control of symptomatic uterovaginal prolapse was significantly reduced compared with that in the remaining 81 women without symptomatic uterovaginal prolapse (0·004 (0·003–0·006) versus 0·019 (0·011–0·037) J respectively; P = 0·02) There was a significant correlation (r = 0·56 (95 per cent confidence interval (c.i.) 0·16 to 0·73); P = 0·006, n = 22) between MRI assessment of uterocervical (median 1·05 (i.q.r. 0·47–1·96) cm) and anorectal (median 1·76 (i.q.r. 0·86–2·37) cm) descent with straining. There was no significant correlation between UsR and either uterocervical descent (r = − 0·30 (95 per cent c.i. − 0·49 to − 0·20); P = 0·11, n = 22) or anorectal descent (r = − 0·34 (95 per cent c.i. − 0·52 to − 0·22); P = 0·11, n = 22). There was a significant correlation between reduced UsR and increasing patient age (Fig. 2 and Table 2). There was a significant decrease in UsR with history of vaginal delivery (Table 2). However, there was no significant difference in UsR (P = 0·48) between women with a history of one (median 0·015 (i.q.r. 0·003–0·026) J; n = 31), compared with two or more (0·017 (0·004–0·035) J; n = 28) vaginal deliveries. There was a significant decrease in UsR with menopause (Table 2). Fig. 2 Open in new tabDownload slide Linear correlation between reduced ligament resilience and increased patient age (r = —0·38 (95 per cent confidence interval—0·55 to—0·17); P < 0·001, n = 81) in women with no history of symptomatic uterovaginal prolapse Table 2 Uterosacral ligament and anterior rectus abdominis sheath resilience, uterosacral ligament thickness, muscle : collagen ratio, oestrogen and progesterone status; by patient age, menopausal status and history of vaginal delivery . Age (years) . Menopause . Vaginal delivery . . ≤ 50 . > 50 . P . Pre . Post . P . No . Yes . P . Uterosacral ligament 0·021 0·012 0·005 0·021 0·013 0·009 0·031 0·015 0·003 resilience (J) (0·015–0·043) (0·004–0·028) (0·015–0·043) (0·004–0·029) (0·019–0·048) (0·004–0·031) Anterior rectus abdominis 0·017 0·029 0·319 0·022 0·029 0·392 0·007 0·030 0·229 sheath resilience (J) (0·006–0·032) (0·015–0·044) (0·007–0·032) (0·009–0·044) (0·006–0·039) (0·014–0·032) Uterosacral ligament 2·8 2·9 0·302 2·9 1·8 0·014 2·8 2·7 0·423 thickness (mm) (2·1–3·7) (2·4–3·8) (2·6–3·8) (1·4–2·7) (1·9–3·2) (2·1–3·8) Uterosacral ligament 0·22 0·21 0·236 0·23 0·21 0·408 0·20 0·22 0·516 muscle : collagen ratio (0·09–0·26) (0·17–0·35) (0·09–0·32) (0·16–0·26) (0·11–0·30) (0·13–0·33) Uterosacral ligament 14 8 0·156 14 8 0·031 8 14 0·267 oestrogen receptors (%) (11–18) (6–14) (6–18) (6–12) (6–13) (6–16) Uterosacral ligament 14 10 0·138 15 10 0·021 13 12 0·498 progesterone receptors (%) (11–18) (8–14) (11–18) (8–13) (8–15) (9–22) . Age (years) . Menopause . Vaginal delivery . . ≤ 50 . > 50 . P . Pre . Post . P . No . Yes . P . Uterosacral ligament 0·021 0·012 0·005 0·021 0·013 0·009 0·031 0·015 0·003 resilience (J) (0·015–0·043) (0·004–0·028) (0·015–0·043) (0·004–0·029) (0·019–0·048) (0·004–0·031) Anterior rectus abdominis 0·017 0·029 0·319 0·022 0·029 0·392 0·007 0·030 0·229 sheath resilience (J) (0·006–0·032) (0·015–0·044) (0·007–0·032) (0·009–0·044) (0·006–0·039) (0·014–0·032) Uterosacral ligament 2·8 2·9 0·302 2·9 1·8 0·014 2·8 2·7 0·423 thickness (mm) (2·1–3·7) (2·4–3·8) (2·6–3·8) (1·4–2·7) (1·9–3·2) (2·1–3·8) Uterosacral ligament 0·22 0·21 0·236 0·23 0·21 0·408 0·20 0·22 0·516 muscle : collagen ratio (0·09–0·26) (0·17–0·35) (0·09–0·32) (0·16–0·26) (0·11–0·30) (0·13–0·33) Uterosacral ligament 14 8 0·156 14 8 0·031 8 14 0·267 oestrogen receptors (%) (11–18) (6–14) (6–18) (6–12) (6–13) (6–16) Uterosacral ligament 14 10 0·138 15 10 0·021 13 12 0·498 progesterone receptors (%) (11–18) (8–14) (11–18) (8–13) (8–15) (9–22) Values are median (interquartile range). Open in new tab Table 2 Uterosacral ligament and anterior rectus abdominis sheath resilience, uterosacral ligament thickness, muscle : collagen ratio, oestrogen and progesterone status; by patient age, menopausal status and history of vaginal delivery . Age (years) . Menopause . Vaginal delivery . . ≤ 50 . > 50 . P . Pre . Post . P . No . Yes . P . Uterosacral ligament 0·021 0·012 0·005 0·021 0·013 0·009 0·031 0·015 0·003 resilience (J) (0·015–0·043) (0·004–0·028) (0·015–0·043) (0·004–0·029) (0·019–0·048) (0·004–0·031) Anterior rectus abdominis 0·017 0·029 0·319 0·022 0·029 0·392 0·007 0·030 0·229 sheath resilience (J) (0·006–0·032) (0·015–0·044) (0·007–0·032) (0·009–0·044) (0·006–0·039) (0·014–0·032) Uterosacral ligament 2·8 2·9 0·302 2·9 1·8 0·014 2·8 2·7 0·423 thickness (mm) (2·1–3·7) (2·4–3·8) (2·6–3·8) (1·4–2·7) (1·9–3·2) (2·1–3·8) Uterosacral ligament 0·22 0·21 0·236 0·23 0·21 0·408 0·20 0·22 0·516 muscle : collagen ratio (0·09–0·26) (0·17–0·35) (0·09–0·32) (0·16–0·26) (0·11–0·30) (0·13–0·33) Uterosacral ligament 14 8 0·156 14 8 0·031 8 14 0·267 oestrogen receptors (%) (11–18) (6–14) (6–18) (6–12) (6–13) (6–16) Uterosacral ligament 14 10 0·138 15 10 0·021 13 12 0·498 progesterone receptors (%) (11–18) (8–14) (11–18) (8–13) (8–15) (9–22) . Age (years) . Menopause . Vaginal delivery . . ≤ 50 . > 50 . P . Pre . Post . P . No . Yes . P . Uterosacral ligament 0·021 0·012 0·005 0·021 0·013 0·009 0·031 0·015 0·003 resilience (J) (0·015–0·043) (0·004–0·028) (0·015–0·043) (0·004–0·029) (0·019–0·048) (0·004–0·031) Anterior rectus abdominis 0·017 0·029 0·319 0·022 0·029 0·392 0·007 0·030 0·229 sheath resilience (J) (0·006–0·032) (0·015–0·044) (0·007–0·032) (0·009–0·044) (0·006–0·039) (0·014–0·032) Uterosacral ligament 2·8 2·9 0·302 2·9 1·8 0·014 2·8 2·7 0·423 thickness (mm) (2·1–3·7) (2·4–3·8) (2·6–3·8) (1·4–2·7) (1·9–3·2) (2·1–3·8) Uterosacral ligament 0·22 0·21 0·236 0·23 0·21 0·408 0·20 0·22 0·516 muscle : collagen ratio (0·09–0·26) (0·17–0·35) (0·09–0·32) (0·16–0·26) (0·11–0·30) (0·13–0·33) Uterosacral ligament 14 8 0·156 14 8 0·031 8 14 0·267 oestrogen receptors (%) (11–18) (6–14) (6–18) (6–12) (6–13) (6–16) Uterosacral ligament 14 10 0·138 15 10 0·021 13 12 0·498 progesterone receptors (%) (11–18) (8–14) (11–18) (8–13) (8–15) (9–22) Values are median (interquartile range). Open in new tab Anterior rectus abdominis sheath resilience There were no significant differences in anterior rectus abdominis sheath resilience by patient age, history of vaginal delivery or menopause (Table 2). There was no significant correlation (r = − 0·03 (95 per cent c.i. − 0·36 to 0·30); P = 0·8, n = 35) between UsR and anterior rectus abdominis sheath resilience. Uterosacral ligament thickness, muscle to collagen ratio, and receptor density Median uterosacral ligament thickness was 2·0 (i.q.r. 1·5–3·0) mm. Reduced ligament thickness significantly correlated with menopause, but not with patient age or vaginal delivery (Table 2). There were no significant differences in uterosacral ligament muscle to collagen ratio by age, menopause or history of vaginal delivery (Table 2). There were significant decreases in oestrogen and progesterone receptor density with menopause, but not with increasing age or history of vaginal delivery (Table 2) There were no significant correlations between UsR and uterosacral ligament thickness (r = 0·16 (95 per cent c.i. − 0·14 to 0·44); P = 0·28, n = 45), muscle to collagen ratio (r = 0·17 (95 per cent c.i. − 0·04 to 0·51); P = 0·25, n = 45), oestrogen receptor density (r = 0·15 (95 per cent c.i. − 0·02 to 0·52); P = 0·34, n = 45) and progesterone receptor density (r = 0·24 (95 per cent c.i. − 0·04 to 0·51); P = 0·18, n = 45). Discussion The fourfold reduction in UsR between the ages of 40 and 80 years suggests that substantial age-related connective tissue weakening17,18 occurs between these ages in female pelvic connective tissues. This age-related pelvic connective tissue degradation could contribute to the late onset of symptomatic visceral prolapse after childbirth16. A pelvic viscus could not prolapse without stretching of attached connective tissue to beyond its plastic limit, and this stretching would be associated with a loss of resilience. This was consistent with the greater than fourfold reduction in UsR in women with symptomatic uterovaginal prolapse. MRI did not suggest pelvic muscle atrophy or weakness38 in the women without symptomatic uterovaginal prolapse. The absence of a significant correlation between reduced UsR and uterocervical or anorectal descent in these women suggests that variation in pelvic connective tissue resilience had little influence on pelvic visceral movement where pelvic muscles were preserved. Significant differences in resilience between left and right uterosacral ligaments were not identified, suggesting that UsR measurement from the right ligament provided valid information. No significant correlation was detected between UsR and anterior rectus abdominis muscle sheath resilience, suggesting that the resilience of abdominal wall connective tissue was not influenced by the same factors as those acting on pelvic connective tissue. Oestrogen and progesterone receptors have been demonstrated within the uterosacral ligament24, and circulating oestrogen levels might influence pelvic connective tissue resilience. In the present study, reductions in both receptor density and UsR occurred with menopause, but the lack of a relationship between oestrogen or progesterone receptor density and UsR did not suggest that reduced uterosacral receptor density mediated a decrease in UsR. UsR was halved in women with a history of vaginal delivery, but no significant reduction was detected with increased number of deliveries. Therefore, UsR reduction may also have been influenced by pregnancy-related39 connective tissue alterations, in addition to the accumulated trauma of vaginal delivery40,41. The thickness of the uterosacral ligament was reduced by 36 per cent with menopause, but no alteration was detected in the ratio of muscle to collagen within the ligament. This suggests that, as with skin20, smooth muscle and collagen were depleted equally within the uterosacral ligament after menopause. The absence of a correlation between UsR and uterosacral ligament thickness suggests that variations in ligament resilience were not explained by smooth muscle and collagen depletion. The menopause-related UsR reduction was more likely to involve qualitative changes in collagen structure42 than simply collagen and smooth muscle depletion. HRT inhibits smooth muscle17,18 and collagen20 degradation in postmenopausal women, and might attenuate the menopause-associated reduction in pelvic connective tissue resilience. Women taking HRT were excluded from the present study. A study assessing whether HRT reduces the postmenopausal decline in UsR, and delays progression to symptomatic pelvic visceral prolapse, would be of interest. Acknowledgements The authors are indebted to the gynaecologists at Chelsea and Westminster Hospital for their cooperation with the study, and to Miss E. Scurr (Superintendent Radiographer) for assistance with MRI. N.H.J.R.J. was supported by a grant from the Chelsea and Westminster Hospital Research Trustees. The authors thank Clare Glover for statistical advice. References 1 Olsen AL , Smith VJ, Bergstrom JO, Colling JC, Clark AL. Epidemiology of surgically managed pelvic organ prolapse and urinary incontinence . Obstet Gynecol 1997 ; 89 : 501 – 506 . Google Scholar Crossref Search ADS PubMed WorldCat 2 Sultan AH , Kamm MA, Hudson CN, Bartram CI. Third degree obstetric anal sphincter tears: risk factors and outcome of primary repair . BMJ 1994 ; 308 : 887 – 891 . 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This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model) Copyright © 2003 British Journal of Surgery Society Ltd. Published by John Wiley & Sons, Ltd.
TI - Pelvic connective tissue resilience decreases with vaginal delivery, menopause and uterine prolapse
JO - British Journal of Surgery
DO - 10.1002/bjs.4065
DA - 2003-03-31
UR - https://www.deepdyve.com/lp/oxford-university-press/pelvic-connective-tissue-resilience-decreases-with-vaginal-delivery-UiX0PC0gRV
SP - 466
EP - 472
VL - 90
IS - 4
DP - DeepDyve
ER -