Obstetrics & Gynecology:
Symptomatic Pelvic Organ Prolapse at Midlife, Quality of Life, and Risk Factors
Fritel, Xavier MD1; Varnoux, Noëlle2; Zins, Marie MD3; Breart, Gérard MD, PhD1; Ringa, Virginie MD, PhD2
From 1Institut national de la santé et de la recherche médicale (INSERM), UMR S149, IFR69, Epidemiological Research on Perinatal Health and Women’s Health, Villejuif, France; Université Pierre-et-Marie-Curie Paris 6, Paris, France; 2INSERM U822-INED U14 “Reproductive health, sexuality, and human immunodeficiency virus (HIV) infection—epidemiology, demography, and social sciences,” Université Paris 11, Le Kremlin-Bicétre, France; and 3INSERM U687-IFR69, “Public health and epidemiology of the social and occupational determinants of Health,” Saint-Maurice, France; Equipe RPPC du Cetaf, Saint-Maurice, France; IFR69, Villejuif, France.
Corresponding author: Dr. Xavier Fritel, Gynécologie & Obstétrique, CHR Réunion, CH Félix-Guyon, F-97405 Saint-Denis cedex, Réunion, France; e-mail: email@example.com.
Financial Disclosure The authors did not report any potential conflicts of interest.
OBJECTIVE: To estimate quality of life, prevalence, and risk factors associated with symptomatic pelvic organ prolapse (POP) among middle-aged women.
METHODS: This was a cross-sectional study. A questionnaire was mailed to 3,114 women aged 50–61 years in the GAZEL cohort; 2,640 (85%) returned it. Symptomatic POP was defined by feeling a bulge from the vagina (sometimes, often, or all the time compared with never or rarely). Quality of life was determined with the Nottingham Health Profile questionnaire. Multiple linear regression was used to examine the association between frequency of POP symptoms and the quality-of-life score. Logistic regression was used to estimate the effect of risk factors on past or present symptomatic POP (current symptoms or previous surgery for POP).
RESULTS: The prevalence of symptomatic POP was 3.6% (96 of 2,640) and that of surgery for POP was 2.7% (70 of 2,640). Pelvic organ prolapse symptoms were associated with difficulty defecating, lower abdominal pain, and difficulty voiding. The frequency of POP symptoms was associated with a poorer quality-of-life score in each Nottingham Health Profile domain (physical mobility, pain, emotional reaction, social isolation, energy, and sleep). Even when we took general characteristics, medical history, and lifestyle associated with quality of life into account, the global Nottingham Health Profile score was significantly impaired by POP symptoms. Factors significantly associated with past or present symptomatic POP were high body mass index and the number of vaginal deliveries.
CONCLUSION: In our population of women in their 50s, POP symptoms are associated with impaired quality of life, and the number of vaginal deliveries is a risk factor for past or present symptomatic POP.
LEVEL OF EVIDENCE: II
The prevalence of pelvic organ prolapse (POP) increases with age and number of vaginal deliveries.1 In the 18th century, Madame du Coudray attributed the onset of a “falling womb” to child birth.2 Despite this association, the mechanism of its onset remains obscure, and we do not know what organ is damaged, let alone how. Although numerous surgical techniques have been developed for POP, epidemiologic surveys on this topic are rare. It is estimated that 15% of all hysterectomies are performed for POP and that the cumulative risk of surgery for POP is approximately 7% at the age of 80 years.3,4 Mean age at this surgery is between 50 years and 60 years of age.5 Despite the frequency of recourse to surgery, the effect of POP on quality of life is not well understood. A MEDLINE search using the terms “quality of life” and “pelvic organ prolapse” showed no studies that examined the deterioration of general health-related quality of life as a function of POP symptoms in a general population, that is, a population not selected because of POP symptoms.
Our main purpose was to estimate the effects of symptomatic POP on quality of life and its prevalence among middle-aged women enrolled in a cohort study and to assess its obstetric risk factors, while taking other characteristics into account. This cohort of French women (GAZEL cohort) completed questionnaires to estimate their general health-related quality of life (Nottingham Health Profile questionnaire) and the frequency of their POP symptoms.
PARTICIPANTS AND METHODS
Our population belongs to the French GAZEL cohort (www.gazel.inserm.fr), which began in 1989 with more than 20,000 men and women employed by the French national power company (EDF-GDF) who volunteered to participate in an epidemiologic research program coordinated by INSERM (Institut National de la Santé et de la Recherche Médicale, that is, the French National Institute for Health and Medical Research).6 Women of the GAZEL cohort aged 45–50 years between 1990 and 1996 (n=3,114) were included in a separate prospective longitudinal survey, the “Women and their Health” study. Its principal objective is to study women’s health as they reach menopause and afterward.7 These women receive a general health questionnaire each year as part of the overall GAZEL survey and a separate questionnaire specific to women’s health issues every 3 years. In 2000, an additional questionnaire about incontinence and obstetric history was mailed to all the women in this survey. Except as otherwise specified, data come from both 2000 questionnaires. The size of our sample was determined by the size of the GAZEL cohort. Three other reports about incontinence based on the same questionnaires and database have previously been published.8–10
At the time this study was initiated, there was no validated questionnaire for assessing pelvic floor symptoms in women without known pelvic floor disorders. The prevalence and severity of symptomatic POP was estimated from responses to the question: In the past 4 weeks, have you experienced the sensation of a bulging from your vagina? Never, Rarely, Sometimes, Often, or All the time. The question was constructed with the help of an expert and was modeled on the Bristol Female Low Urinary Tract Symptoms questionnaire and the Urogenital Distress Inventory11,12 Understanding was not tested. Stress urinary incontinence was assessed by responses to a question from the Bristol Female Low Urinary Tract Symptoms questionnaire: Does urine leak when you are physically active, cough or sneeze? Never, Rarely, Sometimes, Often, or All the time. Women who answered Sometimes, Often or All the time were considered to have stress urinary incontinence. Other pelvic floor symptoms, ie, urinary urge incontinence, voiding difficulties, constipation (fewer than three movements per week), defecation difficulties, lower abdominal pain or heaviness, and pain at intercourse, were assessed by the same method. Fecal incontinence was defined by involuntary loss of liquid or solid stool.
Other characteristics of the subjects considered in this analysis and recorded from the questionnaires (Table 1) are general characteristics (age at questionnaire, educational level, body mass index, and menopausal status), medical history (diabetes mellitus, neurologic disease, cardiovascular disease, regular medical treatment, self-reported nervous breakdown, self-reported depressed mood, anxiety or stress, hysterectomy, previous urinary incontinence surgery, previous anal surgery, and previous POP surgery), lifestyle (household monthly income, marital status, smoking habits, and regular physical exercise), and obstetric history (parity, episiotomy, third-degree perineal tear, birth weight of heaviest child, age at first delivery, and mode of delivery). Previous POP surgery was assessed by the questions: Have you had a surgery? If yes, please specify the type of surgery (a list was provided): pelvic organ prolapse (falling organs) repair? (Yes, No). Self-reported nervous breakdown, and depressed mood, anxiety, or stress were defined by answers to a question presenting a list of health problems and asking the subjects to indicate those they had had during the past 12 months. The list included nervous breakdown as one answer and depressed mood, anxiety, or stress as another. We used logistic regression to examine the association between POP symptoms and other pelvic floor symptoms.
We used the Nottingham Health Profile, a generic instrument widely used to estimate general health-related quality of life and validated in different populations, to determine whether symptomatic prolapse, like other chronic conditions, interferes with everyday life activities.13,14 The Nottingham Health Profile questionnaire was included in the general health questionnaire administered in 2000. It is a generic quality-of-life questionnaire, applicable to a broad range of populations and allowing comparisons between different clinical conditions. The Nottingham Health Profile contains 38 items covering six dimensions: physical mobility (eight items), pain (eight items), emotional reactions (nine items), social isolation (five items), energy (three items), and sleep (five items). The responses are dichotomous (yes/no) and concern the subject’s condition at the time she is completing the questionnaire. A weight is assigned to each response so that a weighted score can be calculated for each of the six dimensions. The weighted scores for each dimension range from 0 (high quality of life) to 100 (low quality of life). Each subject’s profile is described by six scores. It is also possible to construct a global score that is the mean of the six dimensions. We first used the Spearman rank test to analyze the correlation between the quality-of-life scores in each Nottingham Health Profile dimension and the severity of POP symptoms. We then examined the association between the global Nottingham Health Profile score (mean of the scores for each dimension) and the severity of the POP (defined by symptom frequency), using a linear regression to take into account the possible confounding factors: general characteristics, medical history, lifestyle, and parity. We chose not to include in this model other pelvic floor symptoms significantly associated with POP in the preceding analysis.
Past or present symptomatic POP was defined by the report of symptomatic POP or a history of surgery for POP. Because this definition includes surgical history, we chose not to consider in the analysis other surgical history (hysterectomy, surgery for urinary incontinence, and anal surgery), all of which were statistically associated with a history of surgery for prolapse. We compared the women with past or present POP with all the others and conducted a multivariable analysis with a backward step-wise logistic regression. Candidate variables for the multivariable model were those suspected to be risk factors for POP (age, body mass index [BMI], occupation, menopausal status, parity, and mode of delivery) or that could influence symptom reporting (educational level). A first model was constructed for all women. A second model (not shown) was restricted to parous women; it included obstetric details (age at first delivery, birth weight of heaviest baby, episiotomy, and third-degree anal tears). Variables remained in the final multivariable model only if the odds ratio was significant after backward elimination; otherwise, they were excluded.
Odds ratios and their 95% confidence intervals are reported for each association examined. Missing data were less than 10% for each independent variable except for household monthly income (18%) and were not taken into account during analysis. All analyses were performed with Statview (SAS Institute Inc., Cary, NC). The GAZEL cohort scientific committee and the CNIL (Commission Nationale de l’Informatique et des Libertés, that is, the French Data Protection Authority) approved this study, which received no external funding.
Questionnaires were sent to 3,114 women, 2,640 (85%) of whom completed and returned them. Median age was 54 (range 50–61) years and median parity 20–6; 79% were postmenopausal. Respondents and nonrespondents did not differ significantly for age (mean age 54.6 compared with 54.9, P=.14, t test), whereas respondents had a higher educational level than nonrespondents (20% had a high school diploma compared with 15%, P=.012, χ2 test).
The prevalence of symptomatic POP was 3.6% (96), and that of surgery for POP was 2.7% (70). Data about POP symptoms were missing for 193 women (7.3%); 2,296 (87.0%) reported no sensation of a bulge from their vagina in the past 4 weeks, 69 rarely (2.6%), 70 sometimes (2.7%), 18 often (0.7%), and 8 (0.3%) all the time. Additionally, 70 women (2.7%) had previously undergone surgery for POP. Pelvic organ prolapse symptoms were associated with difficulty defecating, lower abdominal pain, and difficulty voiding (Table 2). Other pelvic floor symptoms (stress urinary incontinence, urge urinary incontinence, fecal incontinence, painful intercourse, urinary infection, and fewer than three bowel movements per week) were not significantly associated with POP symptoms after adjustment for difficulty in defecation or voiding and lower abdominal pain.
The Nottingham Health Profile quality-of-life questionnaire was completed by 2,285 women (87%). As Figure 1 shows, the frequency of POP symptoms was associated with increased (that is, poorer) quality-of-life scores in all Nottingham Health Profile dimensions: physical mobility (P<.001), pain (P<.001), emotional reaction (P=.01), social isolation (P=.03), energy (P<.001), and sleep (P=.008). The correlation between the frequency of POP symptoms and quality of life impairment, measured by the global Nottingham Health Profile score, persisted even after adjustments (linear multiple regression) for other factors with a significant effect on quality of life: self-reported nervous breakdown, self-reported depressed mood anxiety or stress, back pain, urge urinary incontinence, few bowel movements, regular physical exercise, hysterectomy, neurologic disease, regular medical treatment, BMI (continuous variable), living as couple, occupation, and monthly income (Table 3). The other variables tested (age, high school diploma, smoking, menopausal status, parity, previous incontinence surgery, previous POP surgery, previous anal surgery, stress urinary incontinence, fecal incontinence, urinary infection, diabetes, and cardiovascular disease) were not significant and were excluded from the final model.
Overall, 158 women (6.0%) were considered to have past or present symptomatic POP. Characteristics associated with it were high BMI and the number of vaginal deliveries (Table 4). The one-variable model that used mode of delivery to predict a history of symptomatic POP had an R2=0.008 (data not shown). The multivariable model for women with children, which also tested age at first delivery, episiotomy, a third-degree anal tear, and birth weight of the largest child, found no other obstetric variable to be significant (data not shown).
In our population of women in their 50s, POP symptoms were associated with a significant impairment of quality of life. Factors associated with past or present symptomatic POP were high BMI and vaginal delivery.
The principal limitation of our study was that POP was not clinically confirmed. Prolapse is a sign observed during clinical examinations, and epidemiologic surveys about this disease are difficult because of the indirectness of its study by questionnaires. Nonetheless, what matters from a practical point of view is symptomatic prolapse that motivates the woman to seek care. That is, women see their doctors for a functional disease and not for an anatomic defect. Moreover, a study of quality of life and the risk factors associated with POP symptoms requires the availability of a sample of women recruited outside of a medical practice. It thus seems useful from a public health perspective to look at the prevalence of prolapse symptoms in the general population.
A major advantage of our sample is that the women participating were not recruited because they had symptoms. Their status as volunteers probably explains the excellent response rate (85%). At the time we began this study, there were no questionnaires validated in a population at low risk for POP.15 Unfortunately, the question we used (Have you experienced a sensation of bulging from your vagina?) could not be combined with clinical examination. Seeing or feeling a vaginal bulge is considered a specific symptom of POP, but the sensitivity of this symptom is mediocre in low-risk populations.16 Barber et al17 showed that the question Do you usually have a bulge or something falling out that you can see or feel in your vaginal area? had a specificity of 99% but a sensitivity of 35% for prolapse at or beyond the hymen (grades II and III) in a population at low risk. The question used by Rortveit et al18 in their study (Has there been a visible bulging or protrusion from your vagina?) had a sensitivity of only 16% for grade II or III prolapse. Symptoms increased with the severity of prolapse; they were frequent for stages III and IV and usually absent at stages I or 0.19 Tan et al20 examined 1,912 women who answered the question: Do you ever feel a bulge or that something is falling out of the vagina? The response was positive in 79–85% of women who had a stage III or IV prolapse compared with 6–11% of women with a stage I or 0. It is therefore probable that those who responded positively in our survey were those with the most serious prolapse. In our study, the bulging symptom was correlated with pelvic pain and difficulties in voiding and defecation (Table 2), which serves as evidence supporting the clinical relevance of the question. Ellerkmann et al21 showed that POP documented by a standardized clinical examination is often associated with these symptoms. Finally, the more frequent the prolapse symptoms, according to this question, the greater the impairment of quality of life in all Nottingham Health Profile dimensions. This graded association between the frequency of prolapse symptoms and quality of life is additional evidence of the question’s clinical relevance.
The relatively rare character of this condition necessarily means that in a general population sample we find few symptomatic women, thus statistical power is limited and significant risk factors more difficult to show. Only 2.7% of our participants had a history of surgery for prolapse and 3.7% had symptoms suggestive of prolapse. These figures are close to those of studies based on clinical examination, which have found only a 0–2.1% prevalence of prolapse beyond the introitus (stage III or IV) in women aged 50–59 years.22,23 The cumulative risk of surgery for POP or urinary incontinence is estimated at 4.7% to 5.1% for women in their 50s.3,24
Another limitation is that our population sample is not exactly representative of middle-aged French women, because women enrolled in the GAZEL cohort were recruited from a work setting and volunteered to participate in medical research. We know, for example, that the women who agreed to participate in GAZEL had a higher education level and were in better health than nonparticipating employees.6–8 From our point of view, that is not likely to affect the quality of life impairment observed or the risk factors identified.
Few studies have examined the effect of POP on quality of life with a generic quality-of-life tool. We showed that the more frequent the prolapse symptoms, the greater the impairment of quality of life in all of the Nottingham Health Profile dimensions. Even in multivariable analysis taking numerous factors likely to be associated with quality of life into account, the symptoms of POP remained associated with a significant impairment in overall quality of life. In the case–control study by Jelovsek et al,25 the Short Form Health Survey (SF-12) physical scale showed impairment in women with prolapse, whereas the mental scale was similar in both groups; this study did not include multivariable analysis. We have previously shown that impairment of quality of life in the Nottingham Health Profile dimensions of physical mobility and pain is proportional to the severity of urinary incontinence.9 A similar result appears for POP symptoms (Fig. 1). This suggests that symptomatic POP can have an important effect on general health-related quality of life and interfere as a disability with physical mobility, pain, emotional reaction, social isolation, energy, and sleep.
We still know very little about its causes. A congenital or acquired tissue factor is probable26–28; the position of the pelvis or the spine may play a role29,30; and physical effort, constipation, a chronic cough, and obesity (BMI is a significant factor in our study) weighing on the pelvic floor may also be involved.31–34 The most frequently suggested hypothesis is that of obstetric trauma. Mant et al33 found a risk of hospitalization for POP proportional to parity. Clinical examination shows that prolapse is more frequent in women with children.22,23 Several other cross-sectional surveys have shown that symptoms of POP are more frequent in women with vaginal deliveries.1,35–37 Nonetheless, the role of vaginal delivery in the natural history of prolapse must be slight, for in our population it explains less than 1% of the symptomatic prolapses. Other mechanisms probably play a role in onset, but we are limited by the cross-sectional nature of our study, which makes it impossible to record the risk factor when it occurs. Only a longitudinal survey can identify traumatic events to the perineum as they occur. In the same GAZEL population, severe stress incontinence (15% prevalence) and fecal incontinence (9.5%) were not associated with mode of delivery.8,10 It is therefore probable that even though these pelvic floor disorders are often associated, they do not share the same pathophysiologic mechanisms. This is consistent with the work by DeLancey et al,38 who showed that stress urinary incontinence is linked more to an aging sphincter than to the impairment of urethral support.
In conclusion, although their prevalence is relatively slight, POP symptoms have a significant effect on the quality of life of the women who have them. Even if it is probable that vaginal delivery plays a role in the genesis of POP, it is an incidental factor that explains only a very small part of it.
1.Rortveit G, Brown JS, Thom DH, van den Eeden SK, Creasman JM, Subak LL. Symptomatic pelvic organ prolapse: prevalence and risk factors in a population-based, racially diverse cohort. Obstet Gynecol 2007;109:1396–403.
2.DuCoudray AM. Abrégé de l’art des accouchements. Châlons-sur-Marne (France): Bouchard; 1773.
3.Carlson KJ, Nichols DH, Schiff I. Indications for hysterectomy. N Engl J Med 1993;328:856–60.
4.Olsen AL, Smith VJ, Bergstrom JO, Colling JC, Clark AL. Epidemiology of surgically managed pelvic organ prolapse and urinary incontinence. Obstet Gynecol 1997;89:501–6.
5.Shah AD, Kohli N, Rajan SS, Hoyte L. The age distribution, rates, and types of surgery for pelvic organ prolapse in the USA. Int Urogynecol J Pelvic Floor Dysfunct 2008;19:421–8.
6.Goldberg M, Chastang JF, Leclerc A, Zins M, Bonenfant S, Bugel I, et al. Socioeconomic, demographic, occupational, and health factors associated with participation in a long-term epidemiologic survey: a prospective study of the French GAZEL cohort and its target population. Am J Epidemiol 2001;154:373–84.
7.Ringa V, Ledésert B, Bréart G. Determinants of hormone replacement therapy among postmenopausal women enrolled in the French GAZEL cohort. Osteoporosis Int 1994;4:16–20.
8.Fritel X, Ringa V, Varnoux N, Fauconnier A, Piault S, Bréart G. Mode of delivery and severe stress incontinence, a cross-sectional study among 2,625 perimenopausal women. BJOG 2005;112:1646–51.
9.Saadoun K, Ringa V, Fritel X, Varnoux N, Zins M, Bréart G. Negative impact of urinary incontinence on quality of life, a cross-sectional study among women aged 49–61 years enrolled in the GAZEL cohort. Neurourol Urodyn 2006;25:696–702.
10.Fritel X, Ringa V, Varnoux N, Zins M, Bréart G. Mode of delivery and fecal incontinence at midlife: a study of 2,640 women in the GAZEL cohort. Obstet Gynecol 2007;110:31–8.
11.Jackson S, Donovan J, Brookes S, Eckford S, Swithinbank L, Abrams P. The Bristol Female Lower Urinary Tract Symptoms questionnaire: development and psychometric testing. Br J Urol 1996;77:805–12.
12.Uebersax JS, Wyman JF, Shumaker SA, McClish DK, Fantl JA. Short forms to assess life quality and symptom distress for urinary incontinence in women: the Incontinence Impact Questionnaire and the Urogenital Distress Inventory. Continence Program for Women Research Group. Neurourol Urodyn 1995;14:131–9.
13.Hunt SM, McEwen J, McKenna SP. Measuring health status: a new tool for clinicians and epidemiologists. J R Coll Gen Pract 1985;35:185–8.
14.Bucquet D, Condon S, Ritchie K. The French version of the Nottingham Health Profile. A comparison of items weights with those of the source version. Soc Sci Med 1990;30:829–35.
15.Baessler K, O’Neill SM, Maher CF, Battistutta D. An interviewer-administered validated female pelvic floor questionnaire for community-based research. Menopause 2008;15:973–7.
16.Doshani A, Teo RE, Mayne CJ, Tincello DG. Uterine prolapse. BMJ 2007;335:819–23.
17.Barber MD, Neubauer NL, Klein-Olarte V. Can we screen for pelvic organ prolapse without a physical examination in epidemiologic studies? Am J Obstet Gynecol 2006;195:942–8.
18.Bradley CS, Nygaard IE. Vaginal wall descensus and pelvic floor symptoms in older women. Obstet Gynecol 2005;106:759–66.
19.Ghetti C, Gregory WT, Edwards SR, Otto LN, Clark AL. Pelvic organ descent and symptoms of pelvic floor disorders. Am J Obstet Gynecol 2005;193:53–7.
20.Tan JS, Lukacz ES, Menefee SA, Powell CR, Nager CW. Predictive value of prolapse symptoms: a large database study. Int Urogynecol J Pelvic Floor Dysfunct 2005;16:203–9.
21.Ellerkmann RM, Cundiff GW, Melick CF, Nihira MA, Leffler K, Bent AE. Correlation of symptoms with location and severity of pelvic organ prolapse. Am J Obstet Gynecol 2001;185:1332–8.
22.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.
23.Samuelsson EC, Victor FT, Tibblin G, Svärdsudd 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.
24.Fialkow MF, Newton KM, Lentz GM, Weiss NS. Lifetime risk of surgical management for pelvic organ prolapse or urinary incontinence. Int Urogynecol J Pelvic Floor Dysfunct 2008;19:437–40.
25.Jelovsek JE, Barber MD. Women seeking treatment for advanced pelvic organ prolapse have decreased body image and quality of life. Am J Obstet Gynecol 2006;194:1455–61.
26.Carley ME, Schaffer J. Urinary incontinence and pelvic organ prolapse in women with Marfan or Ehlers Danlos syndrome. Am J Obstet Gynecol 2000;182:1021–23.
27.Chiaffarino F, Chatenoud L, Dindelli M, Meschia M, Buonaguidi A, Amicarelli F, et al. Reproductive factors, family history, occupation and risk of urogenital prolapse. Eur J Obstet Gynecol Reprod Biol 1999;82:63–67.
28.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.
29.Lazarevski MB. Pelvic morpho-topography and pathogenesis of genital prolapse. Neurourol Urodyn 1999;18:332–3.
30.Mattox TF, Lucente V, McIntyre P, Miklos JR, Tomezsko J. Abnormal spinal curvature and its relationship to pelvic organ prolapse. Am J Obstet Gynecol 2000;183:1381–4.
31.Rinne KM, Kirkinen PP. What predisposes young women to genital prolapse? Eur J Obstet Gynecol Reprod Biol 1999;84:23–5.
32.Jorgensen S, Hein HO, Gyntelberg F. Heavy lifting at work and risk of genital prolapse and herniated lumbar disc in assistant nurses. Occup Med (Lond) 1994;44:47–9.
33.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.
34.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.
35.Lukacz ES, Lawrence JM, Contreras R, Nager CW, Luber KM. Parity, mode of delivery, and pelvic floor disorders. Obstet Gynecol 2006;107:1253–60.
36.Risk factors for genital prolapse in non-hysterectomized women around menopause. Results from a large cross-sectional study in menopausal clinics in Italy. Progetto Menopausa Italia Study Group. Eur J Obstet Gynecol Reprod Biol 2000;93:135–40.
37.Hendrix SL, Clark A, Nygaard I, Aragaki A, Barnabei V, McTiernan A. Pelvic organ prolapse in the Women’s Health Initiative: gravity and gravidity. Am J Obstet Gynecol 2002;186:1160–6.
38.DeLancey JO, Trowbridge ER, Miller JM, Morgan DM, Guire K, Fenner DE, et al. Stress urinary incontinence: relative importance of urethral support and urethral closure pressure. J Urol 2008;179:2286–90.
This article has been cited 5 time(s).
Journal De Gynecologie Obstetrique Et Biologie De La ReproductionPROSPERE randomized controlled trial: Laparoscopic sacropexy versus vaginal mesh for cystocele POP repairJournal De Gynecologie Obstetrique Et Biologie De La Reproduction
International Urogynecology JournalEffect of childbirth on pelvic organ support and quality of life: a longitudinal cohort studyInternational Urogynecology Journal
Neurourology and UrodynamicsPelvic Organ Prolapse and Overactive BladderNeurourology and Urodynamics
Gynecologie Obstetrique & FertilitePelvic floor and pregnancyGynecologie Obstetrique & Fertilite
Bmc Womens HealthImproved quality of life after surgery for pelvic organ prolapse in Nepalese womenBmc Womens Health
© 2009 by The American College of Obstetricians and Gynecologists.