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Positive Symptom Improvement with Laparoscopic Uterosacral Ligament Repair for Uterine or Vaginal Vault Prolapse: Interim Results from an Active Multicenter Trial
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Positive Symptom Improvement with Laparoscopic Uterosacral Ligament Repair for Uterine or Vaginal Vault Prolapse: Interim Results from an Active Multicenter Trial Precis: Laparoscopic uterosacral ligament repair improved symptoms and POP-Q scores long-term in patients with uterine or vaginal vault prolapse while specially designed instrument kits facilitated procedure performance for surgeons. Marlan Schwartz, MD, Karen Rae Abbott, MD, Larry Glazerman, MD, Craig Sobolewski, MD, Barry Jarnagin, MD, Radhika Aliawadi, MD, Vincent Lucente, MD From Lifeline Medical Associates, Piscataway, NJ (Dr. Schwartz), the Athena Gynecology Medical Group, Reno, NV (Dr. Abbott), St. Luke’s Hospital, Allentown, PA (Dr. Glazerman, Dr. Lucente), Vanderbilt University Medical Center (Dr. Jarnigan, Dr. Aliawadi, Duke University Medical Center (Dr. Sobolewski)) KEYWORDS: uterine prolapse, vaginal vault prolapse, uterosacral ligament, laparoscopy Marlan Schwartz, M.D. 64 Stelton Road Piscataway, NJ 08854 Tricountyobj@aol.com 732-968-4444 732-968-1675 This study was funded with an educational grant by Inlet Medical, Inc., a CooperSurgical Company. ABSTRACT STUDY OBJECTIVE: To evaluate the use of laparoscopic uterosacral ligament repair for long-term patient symptom improvement in patients with uterine prolapse or post-hysterectomy vaginal vault prolapse and to evaluate how laparoscopic instrumentation kits facilitate procedure performance for the surgeon. DESIGN: Non-randomized, prospective, multicenter case series SETTING: Five clinical sites consisting of 4 community hospitals and 1 university medical center. DESIGN CLASSIFICATION: II-2 PATIENTS: 72 patients presented with Stage II or worse uterine prolapse (58%, n=42) or post-hysterectomy vaginal vault prolapse (42%, n=30). One patient with Stage I vaginal vault prolapse was included in the group due to her significant symptoms. INTERVENTIONS: Laparoscopic uterosacral ligament repair was performed on all patients; round ligament truncation was also performed selectively on patients with uterine prolapse. Fifty-seven percent (41 patients) had concomitant other pelvic procedures. MEASUREMENTS AND MAIN RESULTS: At 12 months follow-up, POP-Q scores and patient self-reported symptom scores were significantly improved over baseline after laparoscopic pelvic organ prolapse. Positive mean change in POP-Q score was 14.4 (p=.0003) for uterine prolapse repair and 9.28 (p=.017) for vaginal vault prolapse repair. Positive mean change in total symptom score was 20.36 (p<.0001) for uterine prolapse repair and 11.43 (p=.005) for vaginal vault prolapse repair. Surgeons reported a mean procedure time of 31.6 minutes for uterine prolapse repair and 21.7 minutes for vaginal vault prolapse repair. A mean rating of 7.5 was documented for ease of use for the uterine prolapse kit and 4.1 for the vaginal vault prolapse kit on a scale of 1 to 10. CONCLUSION: Laparoscopic uterosacral ligament repair improves symptoms and POP-Q scores long-term in patients with uterine or vaginal vault prolapse. Laparoscopic instrumentation kits facilitate procedure performance for the surgeon with expedited surgery times. INTRODUCTION Pelvic organ prolapse is a serious medical problem for thousands of women in the U.S , , Based on 2001 hospital discharge data, a diagnosis of pelvic organ prolapse was made in approximately 100,000 women, 65 years or older, with 60% of these women presenting with uterine, vaginal wall, or uterovaginal prolapse. One survey of 150,000 women determined that the lifetime risk of undergoing a procedure for prolapse or urinary incontinence was approximately 11% in women with a life expectancy of 80 years. , Moreover, pelvic organ prolapse surgery is responsible for a substantial financial burden on the U.S. health care system, with estimates of approximately $1 billion in annual direct costs. Hysterectomy has been the traditional treatment of choice for women experiencing significant symptoms from uterine prolapse. From 1994 to 1999, prolapse was the third most frequent reason for hysterectomy in the U.S. and the most common reason for hysterectomy in women older than 55 years. Hysterectomy, however, does not eliminate the cause of uterine prolapse and is not an acceptable treatment option for many women. For women of childbearing age, the need for retaining the uterus is obvious, but women choose to avoid hysterectomy for various non-fertility reasons. 8, , The advent of laparoscopic instrumentation and surgical techniques for gynecological procedures has offered minimally invasive alternatives for women in need of surgical interventions for severe pelvic organ prolapse. These techniques use the patient’s own support structures to restore pelvic organs to their normal anatomic positions. Advantages of the laparoscopic approach for the surgeon include superior visualization of pelvic floor anatomy and defects and an enhanced view for more precise suture placement. 12-18 For patients, the laparoscopic approach offers less blood loss, minimized postoperative pain, shorter hospital stays and recovery times, and more cosmetically appealing incisions compared to open surgery. , , , , , , The laparoscopic kit utilized in this study (a product of Inlet Medical) is designed to aid the surgeon in performing the procedure. In recent years, improved laparoscopic instrumentation and techniques have been introduced to facilitate suturing and knot tying, thereby helping to make procedures easier and faster to complete. The purpose of our study was to determine long-term patient symptom improvement from laparoscopic uterosacral ligament support and secondarily to evaluate how instrumentation kits impact procedure times and ease of use for surgeons. In this paper, we present interim results acquired between March 2003 and May 1, 2006 for seventy-two patients. The total study population will consist of 120 patients with sixty uterine prolapse patients and sixty vaginal vault prolapse patients who are followed for a minimum of two years post-procedure. Final results and analysis will be published upon completion of the study. MATERIALS AND METHODS As of May 2006, 72 patients were enrolled in the non-randomized, prospective, multicenter case series. Patients with Stage II or worse on the POP-Q scale for uterine prolapse or post-hysterectomy vaginal vault prolapse were included. One patient with Stage 1 post-hysterectomy vaginal vault prolapse was included due to her significant symptoms. In addition, patients reported at least one of the following symptoms: • Vaginal pain • Vaginal heaviness • Dyspareunia • Anal pain or pressure • Low back pain • Sensation of protrusion Exclusion criteria included current pregnancy, a history of previous repair for uterine or vaginal vault prolapse, and/or unwillingness or inability to participate in follow-up examinations. Each clinical site received approval from their respective IRB (Institutional Review Board). Per IRB-approved protocols, participating patients signed an informed consent at the time of study enrollment. Pre-operatively, all patients underwent a detailed history and physical examination using the POP-Q (Pelvic Organ Prolapse Quantification) system to determine the stage of uterine or vaginal vault prolapse ranging from stage 0, no prolapse to stage 4, complete eversion. For symptom assessment, patients completed a questionnaire using a 10-point, analogue scale to rate 6 symptoms, with 0 indicating no pain or discomfort and 10 representing the worst possible pain or discomfort. The POP-Q scores are isolated to 9 measurements. To analyze as a whole, it was calculated in the following manner. Points Aa, Ba, C, Ap, Bp and D reflect normal support as they become more negative. Therefore, these numbers were reversed as to their value (negatives were positive and vice versa). Points pb and tvl reflect normal support the more positive, thus their numbers were not changed. Finally, only point gh was changed from positive to negative to reflect its superior location in this manner. These numbers were totaled and a total POP-Q score was obtained. Thus, we were able to evaluate all points taken together, which is the anatomic endpoint Clinical investigators performed the surgeries at one of 5 clinical sites throughout the United States. Four were community hospitals and 1 was a university medical center. Investigators at these centers were experienced in laparoscopic treatment of gynecologic conditions, including the treatment of uterine and vaginal vault prolapse. Investigators used one of two all-inclusive procedure kits consisting of instruments specially designed to facilitate pelvic organ prolapse repair. The kit for vaginal vault prolapse differs from the uterine prolapse kit in that the instrument is curved to aid in accessing the uterosacral remnant. Each investigator was asked to measure procedure times and also to rate the kit’s ease of use on a 10-point numeric scale, with 0 indicating greatest difficulty to use and 10 representing greatest ease to use. Patients were followed at 2 weeks, 3 months and 12 months. At the 3 and 12 month visits, each patient underwent a physical examination and was evaluated for POP-Q and symptom scores. POP-Q measurements were reported as absolute values. Individual scores were totaled to obtain a baseline score which was compared with POP-Q scores at follow-up visits. Symptom assessments were based on scores derived from the six-symptom self-reporting analog scale at baseline compared to those at follow-up visits. Surgical Technique Concomitant procedures (e.g., repair of cystocele, rectocele, etc.) were performed before or after proceeding with repair of the uterine or vaginal vault prolapse, per the surgeon’s preference. The appropriate all-inclusive procedure kit was used: the ELEVEST® Procedure Kit (Inlet Medical, Inc. Eden Prairie, MN) for uterine prolapse or the AVESTA® Procedure Kit (Inlet Medical, Inc. Eden Prairie, MN) for vaginal vault prolapse. After induction of general anesthesia, each patient was placed in the dorsal lithotomy position. A uterine manipulator was placed for those patients who were not post-hysterectomy. A 5mm or 10mm infraumbilical vertical incision was made and two 5mm puncture sites were made in the lower abdomen. The patient was then placed in a 5 to 20 degree Trendelenburg position to better visualize the pelvic region and provide the surgeon with better access to the uterine manipulator. Uterosacral Ligament Repair Uterosacral ligament repair was used for both uterine prolapse and vaginal vault prolapse repair. Ureters were identified bilaterally by observing peristalsis, and ureterolysis was performed as necessary to prevent uretral damage or kinking. This was tested by grasping the repair site and checking for tension or tenting of the ureters. The additional port sites allowed for retraction and identification of the ureters, even in the obese patient. Per the surgeon’s choice, either a Prolene suture or a permanent, braided, size 0 suture was grasped in the suture passer and passed through one of the lateral 5mm trocars. The opposite end of the suture was clamped with a hemostat and laid next to the patient. A grasper was introduced through the contralateral trocar. The uterosacral ligaments were identified by visualizing surrounding landmarks (such as the ureter) and then tracing the ligament toward the sacrum. If adhesions in this area were encountered, they were lysed as in any other procedure. Beginning at the distal one-third of the uterosacral ligament and using the grasper to apply counter traction, suture was passed through the ligament, then dropped. The empty suture passer was closed and withdrawn from the ligament. The suture end was grasped and again, the suture passer was directed through the ligament. This was repeated until 3 or 4 sutures were passed through the uterosacral ligament, ending at the cervix or cervical cuff. (Figure 1) The suture ends were both secured with a hemostat to be tied at the end of the procedure. With the same technique, suture was passed through the other uterosacral ligament. An extracorporeal knot was tied and with a knot pusher was used to push down onto the suture to tighten. Several knots were tied to shorten and strengthen the ligament. (Figure 2) Knot tying was repeated on the opposite side. (Figure 3) Round Ligament Repair for Uterine Prolapse When repairing uterine prolapse, surgeons had the option to perform an additional step to invest the round ligament with permanent monofilament suture to bring the uterus into an anteverted position.. Under laparoscopic visualization and with external palpation, the junction of the round ligament and the lateral abdominal wall was identified bilaterally. After infiltration with local anesthetic, a small skin nick was made lateral and superior to the identified junction. INVESTA® suture (Inlet Medical, Inc., Eden Prairie, MN) a monofilament polybutester suture was loaded into the suture passer and passed through the round ligament to 1 cm proximal to the uterus. The suture was dropped and the empty suture passer withdrawn. A second pass was made through the skin nick, cephalad to the first traversing a path on the opposite side of the round ligament. The empty suture passer was passed through the round ligament and exited about 1 cm from the first exit point. The suture end was grasped and withdrawn through the round ligament. The opposite side was completed. Suture ends on both sides were grasped and pulled taut to position the uterus into an anteverted position, with care taken to not over-correct. Sutures were tied and cut, and suture ends were buried within the fascia to prevent skin irritation. (Figure 4) RESULTS A total of 72 patients underwent laparoscopic uterosacral ligament repair from March 2003 to May 2006. All but one patient presented with Stage II or worse on the POP-Q scale. The Stage 1 patient was included because of her self-reported significant symptoms. Forty-two patients (58.7%) had uterine prolapse repair and 30 (41.2%) had vaginal vault prolapse repair. Fifty-seven per cent (41 patients) had other pelvic conditions that were repaired concurrently. Patients may have had more than one concomitant repair, such as cystocele repair, rectocele repair or enterocele repair (Table 1). Patients ranged in age from 30 to 78 years, with a mean of 49 years. Parity ranged from 0 to 5 with a mean of 2.2. (Table 2) Mean BMI was 26.8 kg/m2. Patient demographics were comparable to the demographics of patients reported in other studies of pelvic organ prolapse. 2,3,4, , Mean follow-up time was 46.1 weeks (range 5.9-111.4) for vaginal vault prolapse patients and 26.9 weeks (range 0-109) for uterine prolapse patients. Significant improvements were noted in POP-Q scores between baseline and 12 months for both the uterine prolapse repair from 21.0 to 34.6, p value =.0003 and vaginal vault prolapse repair group from 26.5 to 42.7, p value = .017. (Table 3) Total patient self-reported symptom scores improved significantly from baseline to 12 months for both groups from 22.68 to 2.53, (p value <.0001; 95% CI 14.2-26.5) for uterine prolapse repair and from 18.26 to 3.29, (p value =.005, 95% CI 4.1-18.8) for vaginal vault prolapse repair. Table 4 indicates total changes in symptoms as well as changes in all six symptom categories. Mean procedure time for uterosacral ligament repair for vaginal vault prolapse was 21.7 minutes (range 5-45 min). For uterosacral and round ligament repair for uterine prolapse patients, the mean procedure time was 31.6 minutes (range 16-47 min) (Table 5). The mean ease of use score for the uterine prolapse repair kit was 7.5 and 4.1 for the vaginal vault prolapse repair kit. There were no major complications recorded for any patient. Nine minor events occurred in the vaginal vault support group and twelve occurred in the uterine prolapse group (Table 6). All are known complications of laparoscopic surgery and are not specifically related to pelvic organ prolapse repair. DISCUSSION It is estimated that approximately 11% of women will undergo surgery to correct or repair pelvic organ prolapse before they reach 80 years of age. 5,6 Moreover, pelvic organ prolapse is the third most common reason for hysterectomy in U.S. women 9 and is expected to increase as the U.S. population ages. It has been estimated that nearly 65% of older women (mean age 68 years) in the U.S. have severe uterine prolapse at POP-Q Stage II or III , , although the overall incidence cannot be conclusively determined due to the fact that many women fail to seek treatment. Current medical literature describes a variety of causes for pelvic organ prolapse, including multiple vaginal births, large birth weights, connective tissue weakness, aging, hormonal imbalances, loss of muscle tone, obesity, chronic constipation, heavy lifting or other strenuous activity and family history. 2,3,4,19,20 Various options are available for the treatment of uterine and post-hysterectomy vaginal vault prolapse, ranging from conservative, noninvasive approaches to radical surgical interventions. Conservative treatments such as Kegel exercises or pelvic floor exercises with biofeedback, hormone replacement therapy, and pessaries may be prescribed initially and require patient compliance to maximize success. Exercises, for example, may slow progress of the condition but cannot eliminate it. Hormone replacement therapy has been shown to increase the risk of stroke, blood clots, gallstones, and ovarian cancer. , , The success of vaginal pessaries depends on patient compliance for frequent maintenance to avoid infection, vaginal erosions, and allergic reactions. Hysterectomy has been the traditional treatment for patients with uterine prolapse but for women in their childbearing years, it is not a viable option. Even for older women, loss of the uterus may mean long-term adverse effects, including increased incidences of incontinence and osteoporosis, sexual dysfunction, bowel or urinary tract damage, bladder control problems, constipation, and pelvic pain. Surgical options that preserve the uterus have been limited, and have included the Manchester procedure, fixation of the pelvic structures to the anterior abdominal wall, anchoring of the cervix and/or uterus to the sacral promontory; and transvaginal sacrospinous uterine fixation. 8 Complications associated with these procedures include hemorrhage, visceral injury, uretral injury or kinking, and neurologic impairment. In addition, recurrence of uterine prolapse necessitating reoperation is a concern. The gold standard for vaginal vault prolapse has been the abdominal sacral colpopexy. Colpopexy has a reported success rate of 78-99% but is a complicated and lengthy surgery resulting in significant blood loss and longer hospital stays and recovery times. 6 There have also been higher rates of bowel and ureteral complications reported with this procedure. 23 Laparoscopic uterosacral ligament repair offers a minimally invasive alternative for the treatment of uterine or post-hysterectomy vaginal vault prolapse. This approach has shown success rates between 81 and 100%. 12-18 Benefits of the laparoscopic approach include enhanced visualization of pelvic floor anatomy and defects for surgeons and minimized postoperative pain and recovery times for patients. 12-18 Lin et al 18 retrospectively reviewed 133 patients with uterine or vaginal vault prolapse and found 87.2% (n=116) had no recurrence of prolapse after uterosacral ligament repair with follow-up ranging from 2.0 to 7.3 years. The authors reported a 2.25% complication rate, and there were no ureteral injuries or blood transfusions. In a prospective study of 31 women with an average follow-up of 3.3 years, Yen et al 17 demonstrated that laparoscopic shortening of the uterosacral ligaments, combined with uterine repair, achieved long-lasting results in repositioning the uterus and relieving symptoms. A study of 46 women by Barber et al 13 demonstrated that repair of the vaginal cuff to the uterosacral ligaments, combined with site-specific repair of endopelvic fascia defects, provided excellent anatomic and functional correction of pelvic organ prolapse in most women. McKinney et al 12 successfully performed laparoscopic uterosacral ligament repair in 60 consecutive patients with uterine and vaginal vault prolapse. No subsequent failures were reported up to 4 years post-procedure, and only 11 complications were reported. One challenge associated with the laparoscopic approach for pelvic organ prolapse repair is the potential technical difficulty of suturing. As a result, advanced laparoscopic instrumentation and techniques have been developed to facilitate laparoscopic procedures, particularly in suturing and knot tying. In this report, we present interim results from a non-randomized, prospective, multicenter case series that evaluated long-term improvements in symptom changes and POP-Q scores in 72 patients who underwent uterine prolapse or vaginal vault prolapse repair by surgeons using one of two specially designed instrumentation kits for laparoscopic uterosacral ligament repair procedures (the ELEVEST® and AVESTA® Procedure Kits (Inlet Medical, Eden Prairie, MN). Study results to date demonstrate positive and statistically significant improvements in POP-Q scores and self-reported symptoms between baseline and 12 months. Total symptom score improvement for all six reported symptoms in the uterine prolapse repair group was statistically significant (p value <.0001, 95% CI 14.2-26.5). In addition, surgeons measured procedure time when using the two kits and rated ease of use for each. For laparoscopic uterine prolapse repair, procedure times averaged 31.6 minutes (range 16-47 min.) and ease of use was rated highly for the uterine prolapse procedure kit at mean 7.5 on a scale of 1-10 with 1 being difficult to use and 10 being most ease of use. For those patients with vaginal vault prolapse, the procedure time averaged 21.7 minutes (range 5-45 min) and the procedure kit’s ease of use was rated at 4.1 on the 10 point scale. This may have been due simply to the anatomical difficulties in these post-hysterectomy patients, especially years after hysterectomy. Access with any instrumentation may be problematic and the AVESTA procedure kit provided some additional ease. The procedure kits contained instruments designed to help surgeons with suturing and knot tying. The suture passer enhanced one-directional suture entry through soft tissues and facilitated suture passage while the ligament grasper enhanced tissue holding. The surgical technique included extracorporeal knot tying rather than the more challenging task of intracorporeal knot tying. The knot pusher helped to achieve fast and secure extracorporeal knotting. These procedure kits contributed to easier and faster laparoscopic vaginal organ prolapse repair, potentially expanding the use of uterine-saving procedures for women suffering from debilitating prolapse conditions. Because 12 month results were so positive, the clinical investigator’s group has have submittedsubmitted these interim results for publication. The study end-point is two year follow-up and several patients are already at that stage. While the sample size is relatively small and the data is relatively short term, the trend toward improved symptom and POP-Q scores continues to be positive. An additional 48 patients will continue to be enrolled in the study and final results will be reported once all data are gathered. Finally, because skills vary amongst surgeons in regard to advanced laparoscopy, this kit would likely allow more surgeons to perform this procedure that would not otherwise. Table 1. Per cent patients with concomitant pelvic procedures* PROCEDURE UTERINE PROLAPSE REPAIR (n = 26) VAGINAL VAULT PROLAPSE REPAIR (n = 15) Cystocele repair 44.4 17.9 Rectocele repair 36.6 25 Enterocele repair 28.9 14.3 Adhesion/endometriosis removal 20 10.7 Bladder neck repair 22.2 17.9 Other 32.6 35.7 *Patients may have had more than one of these concomitant procedures. Table 2. Patient demographics UTERINE PROLAPSE REPAIR 58% of patients (n = 42) VAGINAL VAULT PROLAPSE REPAIR 42% of patients (n = 30) Mean age (yr.) 49.1 48.7 Mean parity 2.1 2.4 Table 3. POP-Q score changes from pre-op baseline to 12 months post-op UTERINE PROLAPSE REPAIR n = 42 Pre-op mean (SD) 12 Months Post-op (SD) Mean Change (95% CI) P-value POP-Q Score 21.0 (9.5) 34.6 (9.1) 14.4 (8.1-20.8) 0.0003 VAGINAL VAULT PROLAPSE REPAIR n= 30 Pre-op Mean (SD) 12 Months Post-op (SD) Mean Change (95% CI) P-value POP-Q Score 26.5 (16.0) 42.7 (10.3) 9.28 (2.0-16.6) 0.017 Table 4. Patient self-reported symptom scores pre-op baseline and12 months post-procedure (mean range) SYMPTOM UTERINE PROLAPSE REPAIR (mean range) Baseline (SD) 12 months (SD) Mean Change (95% CI) p-value Total 22.68 (11.5) 2.53 (3.7) 20.36 (14.2-26.5) <.0001 Vaginal pain 1.67 (2.6) 0.25 (1.0) 1.5 (0.6-2.4) 0.002 Vaginal heaviness 5.47 (3.3) 0.63 (1.6) 4.31 (2.5-6.2) 0.0002 Dyspareunia 3.26 (3.8) 0.07 (0.3) 2.86 (0.9-4.8) 0.008 Anal pain 2.6 (3.2) 0.75 (1.5) 1.75 (0.1-3.4) 0.042 Low back pain 3.58 (3.6) 0.56 (1.3) 3.56 (1.7-5.4) 0.0008 Sensation of protrusion 6.7 (3.4) 0.88 (2.1) 5.75 (3.8-7.7) <.0001 SYMPTOM VAGINAL VAULT PROLAPSE REPAIR (mean range) Baseline (SD) 12 months (SD) Mean Change (95% CI) p-value Total 18.26 (11.5) 3.29 (6.2) 11.43 (4.1-18.8) 0.005 Vaginal pain 1.59 (2.4) 0.29 (1.1) 1.36 (-0.2-2.9) 0.08 Vaginal heaviness 3.83 (3.0) 0.43 (1.2) 2.79 (1.1-4.5) 0.004 Dyspareunia 2.33 (2.8) 0.07 (0.3) 1.64 (0.4-2.9) 0.014 Anal pain 2.66 (2.9) 1.14 (2.0) 1.14 (-0.9-3.2) 0.258 Low back pain 3.21 (3.0) 0.79 (1.5) 1.71 (-0.1-3.6) 0.066 Sensation of protrusion 4.76 (3.8) 0.57 (1.5) 2.79 (0.9-4.6) 0.006 Table 5. Physician ratings for procedure kits UTERINE PROLAPSE REPAIR (ELEVEST®) VAGINAL VAULT PROLAPSE REPAIR (AVESTA®) Mean Range Mean Range Procedure Time (min) 31.6 16-47 21.7 5-45 Ease of Use* 7.5 0-10 4.1 1-9 *Physicians’ subjective assessments of ease of use as measured by a 10-point scale, with 0 indicating very difficult to use and 10 indicating very easy to use. Table 6. Reported adverse events ADVERSE EVENT UTERINE PROLAPSE REPAIR # of events (7 patients, 7%) VAGINAL VAULT PROLAPSE REPAIR # events (7 patients, 23%) Incisional and abdominal pain 4 2 Urinary control problems/ bowel strain 0 3 Urinary tract infection 1 1 Infection 0 1 Hemorrhage 1 1 Other 6 1 REFERENCES Brown JS, Waetjen L, Subak L, et al. Pelvic organ prolapse surgery in the United States, 1997. Am J Obstet Gynecol. 2002;186:712-716. Hendrix SL, Clark AC, Nygaard I, et al. Pelvic organ prolapse in the Women’s Health Initiative: gravity and gravidity. Am J Obstet Gynecol. 2002;186:1160-1166. 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Mishra G, Kok H, Ecob R, et al. Cessation of hormone replacement therapy after reports of adverse findings from randomized controlled trials: evidence from a British Birth Cohort. Am J Public Health. 2006;96:1219-1225. Powers K, Lazarou G, Wange A, et al. Pessary use in advanced pelvic organ prolapse. Int Urogynecol J Pelvic Floor Dysfunct. 2006;17:160-164. Danforth KN, Townsend MK, Lifford K, et al. Risk factors for urinary incontinence among middle-aged women. Am J Obstet Gynecol. 2006;194:339-345.
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