Abstract
Objective
Pelvic organ-sparing surgery aims to preserve vital reproductive and sexual organs, enhancing quality of life, especially in premenopausal women. Pelvic organ preservation for female patients undergoing radical cystectomy is now emphasized for sexual and hormonal function. Recent screening studies show no survival advantage despite early diagnosis of ovarian cancer, but opportunistic salpingectomy could reduce high-grade serous carcinoma risk. The aim of this review was to analyze the incidence of metachronous or delayed ovarian cancer in patients undergoing radical cystectomy for bladder cancer.
Methods
PubMed, Scopus, Web of Science, ClinicalTrials.gov, and Cochrane Library were searched systematically for English-language articles up to June 2024. The selection was done first by title and abstract screening and then by full-text assessment for eligibility. This review has been registered in PROSPERO (CRD42024561902).
Results
This review included two retrospective studies (2211 patients). Most patients had local or regional advanced disease, with a minority having distant disease. Only one study reported direct pelvic organ involvement from urothelial cancer, with no ovarian involvement found. Among patients who had organ-sparing surgery or pelvic exenteration, only two developed ovarian cancer post-surgery. No mean follow-up time or side effects from pelvic organ removal were reported in either study.
Conclusion
When oncologically safe, ovarian-sparing surgery with salpingectomy should be considered in female bladder cancer patients undergoing radical cystectomy. Opportunistic salpingectomy should be encouraged during abdominal urological surgeries, with thorough pre-operative counseling guiding decisions. Further studies are needed to define the role of preventive gynecologic surgery in urologic procedures.
Keywords: Prophylactic salpingectomy, Ovarian cancer prevention, Bladder cancer, Cystectomy, Urologic surgery in women
1. Introduction
Pelvic organ-sparing surgery is a surgical approach designed to preserve vital reproductive and sexual organs in women [1]. Maintaining the structural and functional integrity of the organs such as the uterus, ovaries, and vagina can significantly enhance the quality of life post-surgery [2]. The preservation of these organs is particularly crucial for premenopausal women who may wish to retain hormonal function and reproductive potential [3].
As per guidelines, radical cystectomy in female patients encompasses the removal of the bladder, distal ureters, and loco-regional lymph nodes, together with the uterus, adnexa, and anterior portion of the vagina [4,5]. A lot of awareness was raised of the importance of sparing the cervix and of ensuring an adequate vaginal length to preserve sexual function and sexual life in female patients; in selected patients, it has now been accepted to maintain the reproductive organs [4,5]. Recent results from large screening programs failed to demonstrate an advantage in survival despite the increased earlier-stage diagnosis of ovarian cancer [6]. In view of the above, prospective studies demonstrated that opportunistic salpingectomy (OS) could substantially decrease the risk of high-grade serous carcinoma for women in the general population [7].
The aim of this review was to conduct a systematic search of the literature to identify, analyze, and summarize the available studies which report on synchronous or metachronous ovarian cancer development in patients who underwent radical cystectomy or pelvic organ preservation surgery for bladder cancer, respectively.
2. Materials and methods
A systematic search of the literature was performed on PubMed, Scopus, Web of Science, ClinicalTrials.gov, and Cochrane Library for English-language articles published up to June 2024. The search terms used included: OS, prophylactic salpingectomy, salpingectomy, ovarian cancer prevention, female urologic surgery, urologic procedures in women, and urologic surgery. Boolean operators (AND, OR) were used to refine the search.
Supplementary studies were identified by examining the references of systematic reviews and literature reviews. Inclusion criteria were: (1) all age groups; (2) patients with bladder cancer treated with radical surgeries; (3) all techniques of surgeries; and (4) studies available in English. Exclusion criteria encompassed ex vivo or animal studies, preclinical studies, and those classified as case reports, reviews, letters to the editor, or editorial comments. This review has been registered in PROSPERO (registration number CRD42024561902).
2.1. Study selection and data extraction
Two researchers (Cerrato C and Pandolfo SD) independently reviewed all the titles and abstracts retrieved from the search. They then evaluated the full articles of promising studies to choose the final set of studies to be included. Any disagreements between the researchers were resolved by consulting with a senior author (Mir MC).
The following variables were then extracted when available from each of the selected studies: authors, the year and journal of publication, study type, number of patients included in the study, patients' mean age, type of surgery, pathology reports, uterine and/or ovarian and/or vaginal involvement (%, n), pelvic organ preservation surgery, previous sterilization procedure, ovarian cancer development (%, n), and adverse events. Data collection was performed using Microsoft Excel version 16.71 (Microsoft Corporation, Washington, USA), while the analysis was conducted using SPSS v27 (IBM, New York, NY, USA). The quality of evidence and potential biases were assessed using the Grading of Recommendations, Assessment, Development, and Evaluation tool [8] as specified in Supplementary Table 1.
Two reviewers (Cerrato C and Pandolfo SD) independently assessed the risk of bias of each study. Overall, the quality of evidence was graded as “Very low” and the risk of bias was graded as “High” as detailed in Table 1.
Table 1.
Risk of bias and quality of evidence analysis.
| Study, n | Study design | Risk of bias | Inconsistency | Indirectness | Imprecision | Certainty |
|---|---|---|---|---|---|---|
| 2 | Retrospective | High | High | High | High | Very low |
Note: High--further research is very unlikely to change our confidence in the estimate of effect; Moderate--further research is likely to have an important impact on our confidence in the effect and may change the estimate; Low--further research is very likely to have an important impact on our confidence in the estimate of effect and is likely to change the estimate; Very low--any estimate of effect is very uncertain.
3. Results
3.1. Study selection and characteristics
The Preferred Reporting Items for Systematic reviews and Meta-Analyses diagram shows the literature search results (Fig. 1). After excluding all duplicates, 583 papers were screened. After removing the reports that were out of the scope of our systematic review or not in the English language, we identified four papers to be assessed for eligibility. Of these, two papers met the inclusion criteria and were included in the final review.
Figure 1.
The Preferred Reporting Items for Systematic reviews and Meta-Analyses flow diagram for the systematic review.
3.2. Data extraction and analysis
Two articles (2211 patients) were included in this review. Table 2, Table 3 show the summary of the included studies.
Table 2.
The summary of included studies.
Table 3.
Operative, pathologic, and follow-up data.
| Study | Type of surgery, n (%) | Pathology report, n (%) | Uterine involvement, n (%) | Ovarian involvement, n (%) | Vaginal involvement, n (%) | Pelvic organ preservation surgery, n (%) | Preoperative sterilization, n (%) | Ovarian cancer development, n (%) | Adverse event, n (%) | Follow-up, month |
|---|---|---|---|---|---|---|---|---|---|---|
| Salem and El-Mazny, 2012 [10] | RC: 360 (100) |
|
1 (0.28) | 0 (0) | 13 (3.6) | 31 (8.6) | 9 (2.5) | 0 (0) | NS | NS |
| Abboud et al., 2019 [9] | RC: 1851 (100) |
|
NS | NS | NS | NS | NS | 2 (0.11) | NS | NS |
HG, high grade; MIBC, muscle-invasive bladder cancer; NMIBC, non-muscle invasive bladder cancer; NS, not specified; RC, radical cystectomy.
Both studies included were retrospective in their design [9,10]. The mean age was 64.00 (standard deviation 7.07) years. Patients most frequently underwent radical cystectomy or pelvic exenteration including bilateral pelvic lymphadenectomy, hysterectomy, bilateral salpingo-oophorectomy (BSO), urethrectomy, and resection of the upper third of the anterior vaginal wall (n=1881, 85%), either with local or with regional advanced disease (n=2103, 95%), and a minority had distant disease (n=108, 4.9%) [9,10]. Only one study reported the direct impact of urothelial cancer on pelvic organs [10]. In this study, nine patients had a pre-cystectomy sterilization procedure and 31 had an organ-sparing surgery; therefore, for those patients pelvic organs were not included in the sample; one patient had direct uterine involvement from the bladder mass which was not evident at the preoperative CT scan, and 13 had direct vaginal involvement [10]. None of the analyzed samples showed involvement of the ovaries. Of the analyzed specimens, two hundred ninety-three cases were normal and 37 showed benign pathology (fibroids or hyperplasia) [10].
Only one study reports on late ovarian cancer in patients who underwent radical cystectomy for bladder cancer. Two (0.11%) patients developed ovarian cancer at the mean time of 14.5 months after surgery [9]. No mean follow-up time or side effects from pelvic organ removal were reported in either study [9,10].
4. Discussion
Later ovarian disease poses a therapeutic challenge, especially in patients who have undergone radical cystectomy and neo-bladder reconstruction. Using our search strategy, we identified only two studies that aimed to predict the risk of developing synchronous or subsequent ovarian cancer following radical cystectomy for bladder cancer [9,10]. Ovarian metastasis due to the transitional cell carcinoma of the bladder has been summarized in one study, with incidences ranging from 0% to 9% [10]. The primary sites of metastasis for transitional cell carcinoma of the bladder are the pelvic lymph nodes, lungs, bones, and liver [[11], [12], [13]]. In their paper, Bree et al. [14] analyzed the rate of gynecologic organ involvement for women who underwent neoadjuvant chemotherapy and anterior pelvic exenteration for muscle invasive bladder cancer (MIBC) to evaluate the impact of neoadjuvant chemotherapy on gynecological organ involvement, reviewing 186 patients from a single tertiary center treated for cT2–T3 MIBC. They found that at a median follow-up of 32.1 months, no patients had isolated genitourinary recurrence. Salem and El-Mazny [10] in their retrospective analysis, showed that none of the 360 women treated with radical cystectomy for bladder cancer showed ovarian involvement at surgery, and none of the 31 patients whose ovaries were preserved developed ovarian metastasis when bladder cancer recurred. These results were in line with the results of Abboud et al. [9] from the Surveillance, Epidemiology, and End Results database, which reported only two (0.11%) cases of subsequent ovarian cancer after radical cystectomy among all the non-bladder malignancies during the observation period.
Ovarian cancer is generally sporadic. Oophorectomy in premenopausal women is associated with acute premature menopause, increased menopausal symptoms, and a heightened risk of all-cause mortality and cardiovascular disease [[15], [16], [17], [18], [19], [20], [21]]. In both premenopausal and postmenopausal women, it is linked to an elevated risk of osteoporosis [[15], [16], [17], [18], [19], [20], [21]]. Specifically in postmenopausal women, oophorectomy may also increase the risk of cognitive impairment [22] and earlier death [23]. Relative to sexuality, it has been reported that postmenopausal ovaries produce significant amounts of androgens at consistent levels even at older ages [15] and transdermal testosterone treatment after oophorectomy has been demonstrated to improve postoperative sexual function impairment [24]. These data suggest that oophorectomy impairs sexual function in both premenopausal and postmenopausal women, suggesting that preserving the ovaries during radical cystectomy might be preferable for maintaining sexual function at any age, following preoperative counseling regarding sexual function [25]. The prolonged hormone replacement therapy, used to alleviate symptoms and minimize these risks, has been associated with an increased incidence of breast cancer, particularly if used for more than 5 years [26]. Previously, some authors suggested that preserving even just one ovary during radical cystectomy could maintain hormonal function [27], suggesting that preserving one ovary may offer a balance between oncological safety and quality-of-life preservation.
In view of the above, and considering the lack of solid evidence supporting concurrent oophorectomy during radical cystectomy in the general population, in conditions of oncological equipoise, concomitant oophorectomy during radical cystectomy should be recommended for patients who are at risk of ovarian cancer—such as BRCA1 and BRCA2 mutation carriers—since, in this group, it might reduce the risk of ovarian or fallopian cancer by 80% [28,29], while a more conservative approach with ovarian preservation might be considered in the average-risk population.
Nevertheless, epithelial ovarian cancer has the highest mortality rate of all gynecological malignancies, with an overall 5-year survival rate of 30%–40% [30]. The lifetime risk in the general population of ovarian cancer is approximately 1.4%, and among these cases, around 80% are high-grade carcinomas [31]. Emerging evidence suggests that many ovarian cancers originate in the fallopian tubes [[32], [33], [34], [35]], as serous tubal intraepithelial carcinoma is found in approximately 60% of high-grade serous ovarian cancers [36]. Despite advancements, improvements in ovarian cancer treatment and prevention remain limited, underscoring the urgent need for safe and effective preventive strategies.
A growing body of evidence supports the effect of bilateral salpingectomy on reducing ovarian cancer incidence [[37], [38], [39], [40], [41]]. Universal salpingectomy during the simple hysterectomy could potentially prevent 2000 deaths from ovarian cancer in the USA [42]. Several studies have demonstrated that salpingectomy performed for sterilization or other benign indications among the general population conveys an even greater ovarian cancer risk reduction of 42%–47% [37,38], with a specific risk reduction of nearly 80% for serous ovarian and peritoneal cancer in case of OS for non-risk reduction indications [38]. This has been demonstrated by Yoon et al. [43] in a meta-analysis conducted on 77 studies, where they demonstrated a risk reduction of 49% in ovarian cancer risk after bilateral salpingectomy for women who underwent OS (n=29) versus those who did not (n=44) (odds ratio 0.51, 95% confidence interval 0.35–0.75, I2=0%). In Canada, British Columbia's Ovarian Cancer Research team (OVCARE) suggested that gynecologic surgeons should discuss bilateral salpingectomy, for primary prevention of ovarian cancer to all patients who were to undergo hysterectomy [44]. Several studies have demonstrated that OS does not increase the risk of minor complications or adverse events, such as rates of hospital readmission, blood transfusions, or postoperative complications [32,33,45].
The impact of salpingectomy on ovarian function remains unclear. A recent Canadian study found no difference in the time to initiation of hormonal therapy or the first physician visit for menopausal concerns among different OS groups [46]. In contrast, a Swedish registry study reported more menopausal symptoms, and likely hormonal imbalances, 1 year after surgery in women who underwent hysterectomy with OS [47].
Mor-Hadar et al. [48] presented the position statement of the Federation of Gynecology and Obstetrics on OS as an ovarian cancer prevention strategy. They concluded that BSO remains the standard of care to reduce ovarian cancer incidence in high-risk patients, but that the Federation of Gynecology and Obstetrics firmly supports OS, stating that OS becomes an important cancer-risk reducing strategy for average-risk women who have completed their families and are undergoing abdominal or pelvic surgeries, giving the non-gynecological surgical subspecialties an opportunity to decrease the incidence of such a lethal disease and saving lives, provided they collaborate with gynecologic specialists for proper training and patients' counseling [48].
Therefore, OS is a safe procedure without significantly increasing operative time [45,49] and should be offered to all women beyond childbearing age who undergo abdominal surgery for any reason (such as cholecystectomy, hernia repair, appendectomy, and gastrointestinal or urological procedures) [7].
According to patients, their lack of awareness about OS is the key barrier to getting access to the procedure [50], which also reflects a broader lack of knowledge among surgeons. In this respect, in Canada, following OVCARE and subsequent endorsements by the Society of Gynecologic Oncology of Canada and the Society of Obstetricians and Gynecologists of Canada, Hanley et al. [51] examined the rates of OS performed at the time of hysterectomy and how these rates changed over a study period from 2011 to 2016. By 2016, they found more hysterectomies included OS (35.5%) than did not include it (33.5%). However, they estimated that up to 75% of hysterectomies could have included OS, suggesting that surgeons are not uniformly aware of this option or are not consistently discussing OS and its benefits prior to gynecological procedures [51]. Additionally, they noticed a jurisdictional variation of the frequency of OS, with the highest peaks being in those territories with thought leaders and exposure to OS from many different information sources [51,52].
Regarding the urologic community, Sussman et al. [53] conducted an anonymous electronic survey among the Society of Urologic Oncology to assess the knowledge base and practice patterns of urologic oncologists with regard to the management of the gynecological organs at the time of the radical cystectomy. Of the responders, 69% of them were academic urologists and 36% were training urologic oncology fellows; only 14% were aware that salpingectomy alone reduces the risk of ovarian cancer. Awareness of the long-term risks associated with BSO varied: 95% recognized its association with increased osteoporosis risk, 66% with cardiovascular disease, and only 26% with all-cause mortality. The most common reasons cited for performing BSO at the time of RC included concern for urothelial carcinoma metastasis (54%), development of future gynecologic pathology (50%), and facilitation of pelvic lymph node dissection (36%) [53]. All these data suggest that there is an urgent need to educate the urologic community, especially “bladder”-urologic oncologists, who treat bladder cancer, but still remain unaware of the risks associated with BSO and the concept of risk-reducing OS.
Our review has several limitations. First, using our search strategy, we were able to identify only two studies specifically investigating the risk of synchronous or delayed ovarian cancer associated with radical surgeries for bladder cancer. Second, not only the number of studies was limited, but the quality was deemed low, as they were retrospective in nature and/or relied on data from the Surveillance, Epidemiology, and End Results database, which inherently involves assumptions. Third, none of the included studies provided follow-up data, restricting our ability to draw real evidence-based conclusions about the long-term risk and underscoring the need for future research with comprehensive follow-up protocols to address this gap for our female patients in the interest of a more personalized approach to MIBC management and sex-oriented healthcare protocols. Nevertheless, the findings of these studies were supported by previous literature and current guidelines. The major strength of our work is that it sheds light on the necessity for prospective trials investigating the incidence of the gynecologic malignancies in female urologic patients, and it advocates for improvement in the knowledge of the urologic community relative to this topic.
5. Conclusion
In selected cases, when clinically safe and in the context of oncological equipoise, ovarian-sparing surgery with concomitant salpingectomy should be considered in female patients who undergo radical cystectomy for bladder cancer. OS should be encouraged in the urologic community, with shared decision-making guided through preoperative counseling. Further studies are necessary to better define the role of preventive surgery for gynecologic malignancies in the context of urologic surgeries.
Author contributions
Study concept and design: Clara Cerrato, Maria Carmen Mir.
Data acquisition: Clara Cerrato, Savio D. Pandolfo, Pia Kraft.
Data analysis: Clara Cerrato, Savio D. Pandolfo, Maria Carmen Mir.
Drafting of manuscript: Clara Cerrato, Maria Carmen Mir.
Critical revision of the manuscript: Dicken S.C. Ko, Maria Carmen Mir.
Conflicts of interest
The authors declare no conflict of interest.
Footnotes
Peer review under responsibility of Tongji University.
Supplementary data to this article can be found online at https://doi.org/10.1016/j.ajur.2025.03.008.
Appendix A. Supplementary data
The following is the Supplementary data to this article:
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