Year : 2006 | Volume
: 22 | Issue : 4 | Page : 310--316
Pathophysiology of pelvic organ prolapse and stress urinary incontinence
Payal D Patel, Kaytan V Amrute, Gopal H Badlani
Department of Urology, Long Island Jewish Medical Center, USA
Gopal H Badlani
Long Island Jewish Medical Center, Dept. of Urology, 270-05 7 6th Ave, New Hyde Park, NY 11040
Although they may present with significant morbidity, pelvic organ prolapse and stress urinary incontinence are mainly afflicitions that affect quality of life. To appropiately treat these entities, comprehension of the various theories of pathophysiology is paramount. Utilizing a Medline search, this article reviews recent data concerning intrinsic (i.e., genetics, postmenopausal status) and extrinsic factors (i.e., previous hysterectomy, childbirth) leading to organ prolapse or stress incontinence
|How to cite this article:|
Patel PD, Amrute KV, Badlani GH. Pathophysiology of pelvic organ prolapse and stress urinary incontinence.Indian J Urol 2006;22:310-316
|How to cite this URL:|
Patel PD, Amrute KV, Badlani GH. Pathophysiology of pelvic organ prolapse and stress urinary incontinence. Indian J Urol [serial online] 2006 [cited 2020 Dec 1 ];22:310-316
Available from: https://www.indianjurol.com/text.asp?2006/22/4/310/29113
Pelvic organ prolapse is a common and distressing condition. It occurs when there is a weakness in the supporting structures of the pelvic floor allowing the pelvic viscera to descend. While usually not life-threatening, prolapse is often associated with a deterioration in quality of life and may contribute to bladder, bowel and sexual dysfunction. Extended life expectancy and an expanding elderly population mean that prolapse is an increasingly prevalent condition.
Symptoms associated with prolapse are often difficult to correlate with the anatomical site or severity of the 'bulge' and are often nonspecific. Women with prolapse typically complain of the sensation of a 'lump' or vaginal 'heaviness', recurrent irritative bladder symptoms, voiding difficulty, incontinence or defecatory difficulty. Other symptoms such as low back or pelvic pain may or may not be related to prolapse. Surgery for pelvic organ prolapse accounts for approximately 20% of elective major gynecological surgery and this increases to 59% in elderly women. The lifetime risk of requiring surgery for prolapse is 11%, a third of these procedures are operations for recurrent prolapse.
The incidence of urogenital prolapse increases with age. Approximately half of all women over the age of 50 years complain of symptomatic prolapse. One-third of all hysterectomies in postmenopausal women and 81% of vaginal hysterectomies (representing about 16% of all hysterectomies) are performed for prolapse. The yearly incidence of hysterectomy for prolapse peaks in the 65-69-year age group at around 30 per 10,000.
Pelvic organ prolapse is more common following childbirth although it is frequently asymptomatic. Studies have estimated that 50% of parous women have some degree of urogenital prolapse and of these, 10-20% are symptomatic. Only 2% of nulliparous women are reported to have prolapse and this is usually uterine rather than vaginal.
Anatomical Components of the Pelvic Floor
The pelvic floor provides support to the pelvic viscera and consists of the levator ani muscles, urogenital diaphragm, perineal body and endopelvic fascia. The levator ani, when considered with its associated fascia, is termed the pelvic diaphragm. The muscle fibers of the pelvic diaphragm are arranged to form a broad U-shaped layer of muscle with a defect anteriorly. This physiological defect is the urogenital hiatus and allows the passage of the urethra, vagina and rectum through the pelvic floor
Pelvic floor musculature
The muscles of the pelvic floor [Figure 1] are composed of the levator ani and coccygeus, which form a cradle within the bony pelvis supporting the pelvic organs. The levator ani originate on each side from the pelvic sidewall, arising anteriorly just above the arcus tendineus fasciae pelvis (the white line) and inserting posteriorly into the arcus tendineus levator ani. The arcus tendineus fasciae pelvis and arcus tendineus levator ani fuse near the ischial spine. The levator ani has three divisions: the pubococcygeus, ileococcygeus and puborectalis muscles. Ileococcygeus and pubococcygeus arise from the arcus tendineus levator ani fascia overlying obturator internus and insert into the midline anococcygeal raphe and the coccyx. Posteriorly, the coccygeus arises from the ischial spine and sacrospinous ligament and inserts into the coccyx and sacrum.
The striated muscle of the pelvic floor is composed of both slow and fast twitch muscle fibers. The slow twitch fibers provide muscle tone over a long period of time, thus supporting the pelvic viscera while the fast twitch fibers react to sudden increases in intraabdominal pressure.
The urogenital diaphragm (perineal membrane) is a triangular sheet of dense fibrous tissue spanning the anterior half of the pelvic outlet, which is pierced by the vagina and urethra. It arises from the inferior ischiopubic rami and attaches medially to the urethra, vagina and perineal body, thus supporting the pelvic floor.
The perineal body lies between the vagina and the rectum and provides a point of insertion for the muscles of the pelvic floor. It is attached to the inferior pubic rami and ischial tuberosities through the urogenital diaphragm and superficial transverse perineal muscles. Laterally it is attached to the fibers of the pelvic diaphragm while posteriorly it inserts into the external anal sphincter and coccyx.
The endopelvic fascia is a meshwork of collagen and elastin which represents the fused adventitial layers of the visceral structures and pelvic wall musculature. Condensations of the pelvic fascia are termed ligaments and these play an important part in the supportive role of the pelvic floor. The natural 'variation' that exists in the inherent mechanical properties of these and other supportive tissues in the pelvis has been emphasized in recent studies.
Classification of Prolapse
Urogenital prolapse has traditionally been classified by the degree of anatomical deformity, depending on the site of the defect and the presumed pelvic viscera that are involved. The large number of different grading systems that have been used is reflective of the difficulty in designing an objective, reproducible system of grading prolapse. Intra- and interobserver variability is often poor. This makes it difficult to compare successive examinations over time in the same woman or between different women.
Traditional anatomical site prolapse classification
Prolapse of the lower anterior vaginal wall involving the urethra only.
Prolapse of the upper anterior vaginal wall involving the bladder. Generally there is also associated prolapse of the urethra and hence the term cystourethrocele is often used.
This term is used to describe prolapse of the uterus, cervix and upper vagina.
Prolapse of the upper posterior wall of the vagina usually containing loops of small bowel.
Prolapse of the lower posterior wall of the vagina involving the rectum bulging forwards into the vagina.
The other problem with this terminology is that it implies an unrealistic certainty as to the structures on the other side of the vaginal bulge. This is often a false assumption, particularly in women who have had previous prolapse surgery. The terms 'anterior vaginal wall prolapse,' 'posterior vaginal wall prolapse' and 'apical prolapse' are therefore often preferred because of the uncertainty as to the anatomical structures on the other side of the vaginal bulge.
Pelvic organ prolapse quantification (POPQ) scoring system
As a result of these acknowledged problems, the International Continence Society (ICS) has produced a standardized prolapse scoring system, termed the POPQ, in order to assess prolapse more objectively. The POPQ has been shown to have good reproducibility when conducted in a standardized fashion.
The involves the measurement [Figure 2] of set points on the anterior and posterior vaginal walls, cervix and perineal body, against a fixed reference point: the hymen.
Explanation of the POPQ scoring system
The hymen acts as the fixed point of reference throughout the POPQ system.
There are six defined points for measurement in the POPQ system - Aa, Ba, C, D, Ap, Bp. Each is measured in centimeters above or proximal to the hymen (negative number) or centimeters below or distal to the hymen (positive number) with the plane of the hymen being defined as zero (0).
Defined points for measurement in the POPQ system
Anterior vaginal wall:
Point Aa: A point located in the midline of the anterior vaginal wall 3cm proximal to the external urethral meatus. This corresponds to the approximate location of the 'urethrovesical crease,' a visible landmark of variable prominence that is obliterated in many patients. By definition, the range of position of Point Aa relative to the hymen is -3 to +3 cm.
Point Ba: A point that represents the most distal position of the upper portion of the anterior vaginal wall from the vaginal cuff or anterior vaginal fornix to Point Aa. By definition, Point Ba is at -3 cm in the absence of prolapse.
Point C: A point that represents either the most distal edge of the cervix or the leading edge of the vaginal cuff scar in a woman who has undergone total hysterectomy.
Point D: A point that represents the location of the posterior fornix in a woman who still has a cervix. It represents the level of the uterosacral ligament attachment to the proximal posterior cervix.
Posterior vaginal wall:
Point Bp: A point that represents the most distal of the upper portion of the posterior vaginal wall from the vaginal cuff or posterior vaginal fornix to Point Ap. By definition, Point Bp is at -3 cm in the absence of prolapse.
Point Ap: A point located in the midline of the posterior vaginal wall 3 cm proximal to the hymen. By definition, the range of position of Point Ap relative to the hymen is -3 to +3 cm.
Other landmarks and measurements
The genital hiatus (GH): Is measured from the middle of the external urethral meatus to the posterior midline hymen. If the location of the hymen is distorted by a loose band of skin without underlying muscle or connective tissue, the firm palpable tissue of the perineal body should be substituted as the posterior margin for this measurement.
The perineal body (PB): Is measured from the posterior margin of the genital hiatus (as just described) to the midanal opening. Measurement of the genital hiatus and perineal body are expressed in centimeters.
The total vaginal length (TVL): Is the greatest depth of the vagina in cm when Point C or D is reduced to its full normal position.
Etiology of Pelvic Organ Prolapse
Pregnancy and childbirth
Damage to the muscular and fascial supports of the pelvic floor as a result of pregnancy and childbirth contributes to the development of prolapse. In the Oxford Family Planning Association prolapse epidemiology study, parity was the strongest risk factor for the development of prolapse with an adjusted relative risk of 10.9. While the risk increased with increasing parity, the rate of increase slowed after two deliveries. Samuelsson et al . also found statistically significant associations of increasing parity and maximum birth weight with the development of prolapse.
Denervation of the pelvic floor musculature has been shown to occur following childbirth. Gradual denervation has been demonstrated in nulliparous women with increasing age; however, the effects were greatest in those women who had documented stress incontinence or prolapse. Thus it would appear that partial denervation of the pelvic floor is part of the normal aging process, which may be accelerated by pregnancy and childbirth.
'Quality' of connective tissue
The biochemical properties of the connective tissue may also play an important role in the development of prolapse. There is evidence to link clinical and laboratory abnormalities of collagen to pelvic organ prolapse.,,, In addition, Rinne and Kirknen demonstrated an association between prolapse and a history of abdominal herniae in women, suggesting a possible connection with abnormal collagen.
There is a known reduction in tissue collagen content following menopause. Work looking at the expression of estrogen, progesterone and androgen receptors in the levator ani muscles in 55 women undergoing pelvic surgery, showed no expression of estrogen receptors in the levator ani muscle fibers. Interestingly, all types of receptors were identified in the levator ani fascia. Estrogen receptors are found in the vaginal walls and uterosacral ligaments of premenopausal women but reduced in the vaginal walls of postmenopausal women. This is supported by further work demonstrating estrogen receptors in both the cardinal and uterosacral ligaments and there would appear to be a positive correlation with the number of postmenopausal years.
Chronically increased intraabdominal pressure caused by repetitive straining will exacerbate any potential weaknesses in the pelvic floor and is also associated with an increased risk of prolapse. In one case control study, constipation and straining at stool as a young adult before the onset of recognized POP was significantly more common in women who subsequently developed POP (61%) than in women who did not (4%).
Increased stress placed on the musculature of the pelvic floor will exacerbate pelvic floor defects and weakness, thus increasing the incidence of prolapse. Consequently, heavy lifting and exercise as well as sports such as weight lifting, high-impact aerobics and long-distance running increase the risk of urogenital prolapse. A study using the Danish National Registry of Hospitalized Patients included over 28,000 assistant nurses, aged 20-69, who are traditionally exposed to repetitive heavy lifting. Their risk of surgery for prolapse and herniated lumbar disc was compared to the risk in over 1.6 million same-aged controls. The odds ratio for the nurses compared to controls was 1.6 (1.3-1.9) for prolapse surgery and 1.6 (1.2-2.2) for disc surgery, suggesting that heavy lifting is a significant risk factor.
Previous pelvic surgery
Past surgery may also have an effect on the incidence of developing prolapse. Continence procedures, while elevating the bladder neck, may lead to defects in other pelvic compartments. Burch colposuspension, by fixing the lateral vaginal fornices to the ipsilateral iliopectineal ligaments, leaves a potential defect in the posterior vaginal wall, which predisposes to rectocele and enterocele formation. In a five-year follow-up study of women, 36% had cystoceles, 66% rectocele, 32% enterocele and 38% uterine prolapse. A further series of 109 women with vaginal vault prolapse reported that 43% had previously undergone Burch colposuspension. Overall, 25% of women following Burch colposuspension required further surgery for prolapse. Needle suspension procedures and sacrospinous ligament fixation are also associated with an increased incidence of recurrent prolapse.
The association between prolapse and prior hysterectomy is not as clear. Swift also demonstrated a significant association of prolapse with a prior history of hysterectomy or prolapse surgery. One large series reported vaginal vault prolapse 9-13 years after hysterectomy in 11.6% of women who had the hysterectomy for prolapse and in 1.8% of women who had the hysterectomy for their benign disease. However, other factors such as the aging process and estrogen withdrawal following menopause may also have an important role.
Most women complain of a feeling of discomfort or heaviness within the pelvis in addition to a 'lump coming down.' Symptoms tend to become worse with prolonged standing and towards the end of the day. They may also complain of dyspareunia, difficulty in inserting tampons and chronic lower backache. In cases of advanced, long-term prolapse there may be epithelial ulceration and lichenification [Figure 3] that results in a symptomatic vaginal discharge or bleeding. Pelvic organ prolapse may be associated with lower urinary tract symptoms of urgency and frequency of micturition in addition to a sensation of incomplete emptying which may be relieved by digitally reducing the prolapse. One study noted that the majority of women with symptomatic prolapse still void effectively. Fitzgerald found that preoperative voiding studies with the prolapse reduced by a pessary was the best predictor of normal voiding postoperatively.
An abdominal examination should be performed to exclude the presence of an abdominal or pelvic tumor that may be responsible for the prolapse. Pelvic examination to assess the degree of prolapse is usually performed with the women in either the left lateral position using a Simms' speculum or in a semirecumbent position in an examination chair. In addition, digital examination of the woman in a standing position allows an accurate assessment of the degree of urogenital prolapse and in particular of vaginal vault support.
In women who also complain of concomitant lower urinary tract symptoms, urodynamic studies or a postmicturition bladder ultrasound should be performed in order to exclude a chronic residual due to associated voiding difficulties. In such cases a midstream specimen of urine should be sent for culture and sensitivity. Since occult urodynamic stress incontinence may be unmasked by straightening the urethra following surgical repair of the anterior vaginal wall, this should be simulated by the insertion of a ring pessary or tampon to reduce the cystocele. Studies have described an occult stress incontinence rate after various methods of reducing the prolapse, during preoperative testing, of 23-50%. If stress incontinence is demonstrated then the possibility of performing a simultaneous continence procedure, such as colposuspension or insertion of tension-free vaginal tape (TVT) should be discussed.
In cases of severe prolapse in which there may be a degree of ureteric obstruction, it is important to evaluate the upper urinary tract either with a renal tract ultrasound or intravenous urogram.
In general any factor that leads to chronic increases in abdominal pressure should be avoided. Consequently, care should be taken to avoid constipation, which has been implicated as a major contributing factor to urogenital prolapse in the Western society. In addition, the risk of prolapse in patients with chronic chest pathology such as obstructive airways disease and asthma should be reduced by effective management of these conditions. Hormone replacement therapy may theoretically also decrease the incidence of prolapse, although to date there are no studies that have tested this effect. Smaller family size and improvements in antenatal and intra-partum care have been implicated in the primary prevention of urogenital prolapse. The role of cesarean section may also be important. One large study of over 21,000 Italian women demonstrated a significant association between vaginal delivery and subsequent uterine prolapse. Antenatal and postnatal pelvic floor muscle training has not yet been shown to conclusively reduce the incidence of prolapse, although there are logical reasons to think that it may be protective.
Pelvic floor muscle training has a role in cases of mild prolapse, especially in younger women who have not yet completed their family and may find an intravaginal device unacceptable. Education about pelvic floor exercises may be supplemented with the use of a perineometer and biofeedback allowing quantification of pelvic floor contractions. In addition, vaginal cones and electrical stimulation may be used.
Intravaginal devices are available in a wide variety of sizes and designs. Ring pessaries made of silicone or polythene are currently the most frequently used. They are available in a number of different sizes (52-120 mm) and are designed to lie horizontally in the pelvis with one side in the posterior fornix and the other just behind the pubis, hence providing support for the uterus and upper vagina. Fitting is usually done by trial and error. A properly fitted pessary should allow a finger to fit between the pessary and the vaginal wall, thus aiding and ensuring easy removal. Wood advises starting with the largest pessary that can be comfortably admitted into the introitus but not protrude out of the orifice. A vaginal lubricant is usually applied to the pessary surface to minimize the discomfort of fitting. Pretreatment with vaginal estrogen for two to three weeks prior to the insertion appointment is the best way to enhance vaginal lubrication, to decrease atrophy and thereby minimize discomfort at the time of fitting.
Pessaries should be changed every six months and long-term use may be complicated by vaginal ulceration and hence a low-dose topical estrogen may be helpful for postmenopausal women.
Pessaries offer an effective conservative line of therapy for women who do not wish to undergo or are unfit for surgery. They are also suitable for women who suffer with pelvic organ prolapse during pregnancy and the puerperium and may offer symptomatic relief while for women awaiting surgery.
Surgery offers definitive treatment of urogenital prolapse. It offers the best chance of a long-term cure, but as with all forms of surgical treatment it is not entirely risk-free. In particular, the risk of postoperative dyspareunia, both in the short term and occasionally as a long-term complication, need to be discussed. As in other forms of pelvic surgery, patients should receive prophylactic antibiotics to reduce the risk of postoperative infection, as well as thromboembolic prophylaxis in the form of low-dose heparin and antithromboembolic (TED) stockings. All women should also have a urethral catheter inserted at the time of the procedure unless there is a particular history of voiding dysfunction and in which case a supra-pubic catheter may be more appropriate. This allows the residual urine volume to be checked following a void without the need for recatheterization. Women having pelvic floor surgery are positioned in lithotomy with hips abducted and flexed. To minimize blood loss, local infiltration of the vaginal epithelium is performed using 0.5% xylocaine and 1/200,000 adrenaline, although care should be taken in patients with coexistent cardiac disease. At the end of the procedure a vaginal pack may be inserted and removed on the first postoperative day. Step-by-step methodology for the various operations that have been described for correcting prolapse is beyond the scope of this article but is well covered in the standard gynecology textbooks. Below is a summary of some of the more widely performed operations and their indications.
Anterior compartment defects
Anterior colporrhaphy: For correction of cystourethrocele
Paravaginal repair: For correction of cystourethrocele
Posterior compartment defects
Posterior colporrhaphy: For correction of rectocele and deficient perineum
Enterocele repair: For correction of enterocele
Vaginal hysterectomy: For repair of uterovaginal prolapse.
May be combined with anterior and posterior colporrhaphy.
Sacrospinous ligament fixation: For vaginal vault prolapse
Abdominal sacrocolpopexy: For vaginal vault prolapse
Recurrent urogenital prolapse
Approximately one-third of the operations for urogenital prolapse are for recurrent defects. Recurrent prolapse may occur following both abdominal and vaginal hysterectomy, previous vaginal repairs and continence surgery. In addition, women with intrinsically weak connective tissue are at increased risk.,
In such cases the vaginal epithelium may be scarred and atrophic, making surgical correction technically more difficult and increasing the risk of damage to the bladder and bowel. The risk of postoperative complications such as dyspareunia secondary to vaginal shortening and stenosis is also increased.
In recent years there has been an increasing interest in the use of biological and synthetic surgical meshes to reinforce traditional reconstructive techniques. These materials theoretically offer additional support in cases where the endopelvic fascia and vaginal epithelium are intrinsically weak.
The use of prosthetic mesh was pioneered by general surgeons for the repair of abdominal wall herniae and it was adapted for use in vaginal surgery. However, unlike the anterior abdominal wall, the vagina is a tubular structure and it is important not to compromise vaginal capacity, elasticity or sensation if sexual function is to be adequately retained. In reconstructive pelvic surgery, biological and synthetic prostheses have been commonly employed for suspending the vaginal vault as part of an abdominal sacrocolpopexy operation, since this was first described by Lane in 1962. Reinforcement of the anterior and posterior vaginal walls with mesh as part of a vaginal pelvic floor repair is a more recent phenomenon. There is emerging evidence to suggest a role for the use of surgical meshes in vaginal repair surgery, but the ideal material and patient group have yet to be firmly established. Synthetic prosthetic meshes may be classified into Types I-IV, according to the type of material, pore size and whether they are monofilament or multifilament. Current evidence would favor the use of Type I polypropylene meshes on the basis of lower infection and erosion rates, but there is a desperate need for further randomized controlled trials to determine long-term efficacy and potential morbidity associated with the use of these materials.
In one of the very few randomized controlled trials conducted in this area of interest, Sand demonstrated significantly lower recurrence rates at 12 months follow-up in 161 women with cystoceles (140 primary and 21 recurrent) undergoing fascial plication with mesh reinforcement of the anterior vaginal wall (25%), compared to those undergoing fascial plication alone (43%). No mesh-related complications were reported during this trial. Elsewhere, the published incidence of mesh-related complications varies greatly. Dyspareunia is a common complication associated with the use of synthetic mesh and may be associated with erosion into the vagina, lower urinary tract and rectum. Erosion rates as high as 25% and severe dyspareunia precluding the resumption of sexual intercourse have been reported.  Managing some of the postoperative complications associated with the use of nonabsorbable synthetic prostheses can prove very difficult.
While not life-threatening, urogenital prolapse is responsible for significant morbidity and impairment of quality of life. With approximately half of elective gynecological operations being performed for correction of urogenital prolapse, the economic considerations are also considerable. Although conservative measures may be useful in the management of mild symptomatic prolapse, surgery offers the definitive treatment. Women should be carefully assessed with regard to their symptoms and how these impact on their quality of life prior to any surgical treatment. As with surgery for female stress incontinence, the primary procedure offers the greatest probability of success and it is important that women are given realistic figures on the likely outcome of surgical intervention. The large number of surgical procedures described is indicative of the fact that there is no perfect solution. This is also reflected in the number of patients who present with recurrent prolapse. Such women should be managed in tertiary units by surgeons with a specialist interest in pelvic floor reconstructive surgery. The use of synthetic meshes to augment traditional prolapse repair operations is an exciting development, but as yet there is little robust evidence to support its widespread use.
|1||Swift SE, Tate SB, Nicholas J. Correlation of symptoms with degree of pelvic organ support in a general population of women: What is pelvic organ prolapse? Am J Obstet Gynecol 2003;189:372-9.|
|2||Olsen AL, Smith VG, Bergstrom JO, Colling JC, Clark AL. Epidemiology of surgically managed pelvic organ prolapse and urinary incontinence. Obstet Gynecol 1997;89:501-6.|
|3||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;183:277-85.|
|4||Allard P, Rochette L. The descriptive epidemiology of hysterectomy, province of Quebec, 1981-1988. Ann Epidemiol 1991;1:541-9.|
|5||Progetto Menopausa Italia Study Group. Risk factors for genital prolapse in non-hysterectomized women around menopause, results from a large cross-sectional study in menopausal clinics in Italy. Eur J Obstet Gynecol Reprod Biol 2000;93:125-40.|
|6||Samuelsson EC, Victor FT, Tibblin G, Svardsudd KF. 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;180:299-305.|
|7||Dietz HP, Hansell NK, Grace ME, Eldridge AM, Clarke B, Martin NG. Bladder neck mobility is a heritable trait. BJOG 2005;112:334-9.|
|8||Abrams P, Blaivas JG, Stanton SL, Andersen JT. The International Continence Society Committee on Standardization of Terminology. The standardization of terminology of terminology of lower urinary tract function. Scand J Urol Nephrol 1988;114:5-19.|
|9||Mant J, Painter R, Vessey M. Epidemiology of genital prolapse:observations from the Oxford Family Planning Association study. Br J Obstet Gynaecol 1997;104:579-85.|
|10||Snooks SJ, Swash M, Henry MM, Setchel M. Risk factors in childbirth causing damage to the pelvic floor innervation. Int J Colorectal Dis 1986;1:20-4.|
|11||Smith AR, Hosker GL, Warrell DW. The role of partial denervation of the pelvic floor in the aetiology of genitourinary prolpase and stress incontinence. A neurophysiological study. Br J Obstet Gynaecol 1989;96:24-8.|
|12||Al-Rawizs S, Al-Rawizs T. Joint hypermobility in women with genital prolapse. Lancet 1982;26:1439-41.|
|13||Marshman D, Percy J, Fielding I, Delbridge L. Rectal prolapse: Relationship with joint mobility. Aust N Z J Surg 1987;545:827-9.|
|14||Norton P, Boyd C, Deak S. Collagen synthesis in women with genital prolapse or stress urinary incontinence. Neurourol Urodyn 1992;11:300-1.|
|15||Jackson SR, Avery NC, Tarlton JF, Eckford SD, Abrams P, Bailey AJ. Changes in metabolism of collagen in genitourinary prolapse. Lancet 1996;347:1658-61.|
|16||Rinne KM, Kirkinen PP. What predisposes young women to genital prolapse? Eur J Obstet Gynecol Reprod Biol 1999;84:23-5.|
|17||Copas P, Bukovsky A, Asbury B, Elder RF, Caudle MR. Estrogen, progesterone and androgen receptor expression in levator ani muscle and fascia. J Womens Health Gend Based Med 2001;10:785-95.|
|18||Chen GD, Oliver RH, Leung BS, Lin LY, Yeh J. Estrogen receptor a and b expression in the vaginal walls and uterosacral ligaments of premenopausal and postmenopausal women. Fertil Steril 1999;71:1099-102.|
|19||Lang JH, Zhu L, Sun ZJ, Chen J. Estrogen levels and estrogen receptors in patients with stress urinary incontinence and pelvic organ prolapse. Int J Gynaecol Obstet 2003;80:35-9.|
|20||Lubowski DZ, Swash M, Nichols RJ, Henry MM. Increases in pudendal nerve terminal motor latency with defecation straining. Br J Surg 1988;75:1095-7.|
|21||Spence-Jones C, Kamm MA, Henry MM, Hudson CN. Bowel dysfunction: A pathogenic factor in uterovaginal prolapse and urinary stress incontinence. Br J Obstet Gynaecol 1994;101:147-52.|
|22||Jorgensen S, Hein HO, Gyntelberg F. Heavy lifting at work and risk of genital prolapse and herniated lumbar disc in assistant nurses. Occup Med 1994;44:47-9.|
|23||Wiskind AK, Creighton SM, Stanton SL. The incidence of genital prolapse after the Burch colposuspension. Am J Obstet Gynecol 1992;167:399-405.|
|24||Bump RC, Hurt WG, Theofrastous JP, Addison WA, Fantl JA, Wyman JF, et al . Randomized prospective comparison of needle colposuspension versus endopelvic fascia plication for potential stress incontinence prophylaxis in women undergoing vaginal reconstruction for stage III or IV pelvic organ prolapse. Am J Obstet Gynecol 1996;175:326-35.|
|25||Marchionni M, Bracco GL, Checcucci V, Carabaneanu A, Coccia EM, Mecacci F, et al . True incidence of vaginal vault prolapse: Thirteen years experience. J Reprod Med 1999;44:679-84.|
|26||Coates KW, Harris RL, Cundiff GW, Bump RC. Uroflowmetry in women with urinary incontinence and pelvic organ prolapse. Br J Urol 1997;80:217-21.|
|27||FitzGerald MP, Kulkarni N, Fenner D. Postoperative resolution of urinary retention in patients with advanced pelvic organ prolapse. Am J Obstet Gynecol 2000;183:1361-4.|
|28||Chaikin DC, Groutz A, Blaivas JG. Predicting the need for antiincontinence surgery in continent women undergoing repair of severe urogenital prolapse. J Urol 2000;163:531-4.|
|29||Gallentine ML, Cespedes RD. Occult stress urinary incontinence and the effect of vaginal vault prolapse on abdominal leak point pressures. Urology 2001;57:40-4.|
|30||Wood N. The use of vaginal pessaries for uterine prolapse. Nurse Pract 1992;17:31-8.|
|31||Lane FE. Repair of posthysterectomy vaginal vault prolapse. Obstet Gynecol 1962;89:501-6.|
|32||Julian TM. The efficacy of Marlex mesh in the repair of severe recurrent vaginal prolapse of the anterior mid vaginal wall. Am J Obstet Gynecol 1996;175:1472-5.|
|33||Amid P. Classification of bio materials and their related complications in abdominal wall surgery. Hernia 1997;1:15-21.|
|34||Sand PK, Koduri S, Lobel RW, et al . Prospective randomised trial of Polyglactin 910 mesh to prevent recurrences of cystoceles and rectoceles. Am J Obstet Gynecol 2001;185:1229-307.|
|35||de Tayrac R, Gervaise A, Fernandez H. Tension-free polypropylene mesh for vaginal repair of severe anterior vaginal wall prolapse. Int Urogyn J 2002;13:S41.|