INTRODUCTION — Opportunistic salpingectomy (OS) is the removal of the fallopian tubes for primary prevention of epithelial ovarian, fallopian tube, and peritoneal carcinoma in a patient at average risk for these cancers and undergoing pelvic surgery for another indication. By contrast, risk-reducing bilateral salpingo-oophorectomy (rrBSO) is a procedure performed in patients at high risk for these cancers.
The preventive strategy of OS is based on an abundance of data demonstrating that the fallopian tubes, rather than the ovaries, are the primary site of most epithelial ovarian, fallopian tube, and peritoneal carcinomas. Salpingo-oophorectomy, rather than salpingectomy alone, is not considered part of primary prevention in premenopausal patients, as oophorectomy results in loss of ovarian function and is associated with long-term health risks.
OS for epithelial ovarian, fallopian tube, and peritoneal carcinoma risk reduction in average-risk patients is reviewed here. Risk-reducing salpingo-oophorectomy for patients at high risk for these cancers is discussed separately. (See "Risk-reducing salpingo-oophorectomy in patients at high risk of epithelial ovarian and fallopian tube cancer".)
OVERVIEW AND RATIONALE — Epithelial ovarian carcinoma (EOC) is not a single disease but rather consists of five different histotypes; in order of frequency, they include high-grade serous, endometrioid, clear cell, low-grade serous, and mucinous carcinomas. Because of their common features, high-grade serous ovarian, fallopian tube, and peritoneal carcinoma are considered one clinical entity and referred to as a single entity (EOC). (See "Epithelial carcinoma of the ovary, fallopian tube, and peritoneum: Histopathology".)
In 2010, the British Columbia Ovarian Cancer Research (OVCARE) team proposed prophylactic salpingectomy as a strategy for primary prevention of EOC [1]; this was based on the following observations:
Role of the fallopian tube in carcinogenesis — The majority of EOCs arise from the epithelium of the distal fallopian tube rather than the ovary itself [2-4]. These findings may account for the observed residual risk of peritoneal high-grade serous carcinoma following oophorectomy without removal of the fallopian tubes [5-7]. (See "Epithelial carcinoma of the ovary, fallopian tube, and peritoneum: Histopathology".)
In addition, in patients at high risk for EOC (eg, patients with BRCA1 and BRCA2 mutations) undergoing risk-reducing bilateral salpingo-oophorectomy (rrBSO), occult fallopian tube carcinomas and/or preinvasive lesions in the distal fallopian tubes (serous tubal intraepithelial carcinoma [STIC]) has been described; however, intensive examination of the ovaries in these patients have failed to find premalignant or malignant epithelial changes [8-15]. (See "Risk-reducing salpingo-oophorectomy in patients at high risk of epithelial ovarian and fallopian tube cancer", section on 'Counseling and consent'.)
Preinvasive lesions have also been found in fallopian tube specimens of average-risk patients who have not yet developed cancer, although this is rare [16-19]. These tubal specimens are typically from patients who underwent sterilization or hysterectomy for benign indications. Many or most of these patients are younger than 65 years, which is the average age of diagnosis of ovarian cancer in the general population. Thus, the low incidence of STICs in this population is not surprising.
An important component of the studies of rrBSO specimens has been the use of the Sectioning and Extensively Examining the Fimbria (SEE-FIM) protocol, which is a technique for sectioning and examination of the fallopian tube to maximize the detection of neoplasia [8,20]. Using this protocol, tubal involvement has been found in up to 75 percent of patients diagnosed with ovarian or primary peritoneal high-grade serous carcinoma (with and without BRCA mutations) [21-23], including the presence of fimbrial STICs in 40 to 60 percent [23-27].
Efficacy of tubal ligation in cancer reduction — Tubal ligation has consistently been shown to decrease the risk of developing EOC [28-41], with large retrospective studies reporting a greater risk reduction for nonserous cancers, particularly endometrioid and clear cell histotypes [34-36], than for serous cancers [35].
Possible mechanisms for risk reduction include the following: removing the initial site of carcinogenesis (high-grade serous carcinomas) [42]; removing the conduit for passage of endometriotic or endosalpingiotic cells (clear cell and endometrioid carcinomas) [43-45]; and removing the conduit for passage of carcinogens (eg, talc) or inflammation (eg, pelvic infection) to reach the ovary. However, the role of these factors is not well established. (See "Endosalpingiosis" and "Epithelial carcinoma of the ovary, fallopian tube, and peritoneum: Incidence and risk factors", section on 'Talc'.)
Tubal ligation techniques include surgical clips or rings, cauterization, or partial salpingectomy. While most studies of tubal ligation and EOC do not report results for specific methods of tubal ligation, hysteroscopic tubal ligation methods are generally not included in these studies. (See "Overview of female permanent contraception".)
The role of complete salpingectomy in cancer reduction is discussed in detail below. (See 'Ovarian cancer risk reduction' below.)
Other
●Limitations in early detection and poor prognosis – In general, EOC presents at an advanced stage and has a poor prognosis (table 1 and table 2). The overall survival rate for patients with ovarian cancer has remained largely unchanged since the mid-1980s [46-50]. While clinical trials show that use of a poly (ADP-ribose) polymerase (PARP) inhibitor as maintenance therapy affords a progression-free survival advantage in select patients [51-54], whether it affords an overall survival advantage has not been reported, as data are immature. (See "Epithelial carcinoma of the ovary, fallopian tube, and peritoneum: Incidence and risk factors", section on 'Incidence' and "Overview of epithelial carcinoma of the ovary, fallopian tube, and peritoneum", section on 'Prognosis' and "First-line chemotherapy for advanced (stage III or IV) epithelial ovarian, fallopian tube, and peritoneal cancer", section on 'PARP inhibitors'.)
●Limitations in screening – Various screening tools for ovarian cancer have not been shown to improve cancer-specific mortality. In the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS) trial including over 202,000 postmenopausal patients followed for a median of 16 years, those undergoing annual screening (ie, multimodal, transvaginal ultrasound) versus no screening had similar rates of death from ovarian or tubal carcinomas [55]. This is discussed in more detail separately. (See "Screening for ovarian cancer", section on 'Lack of benefit of screening strategies'.)
For patients who present with signs or symptoms suggestive of ovarian cancer, evaluation may include serum biomarkers and pelvic imaging, but the specificity of these tests is low and many patients with benign adnexal masses undergo unnecessary surgeries [56-60]. (See "Approach to the patient with an adnexal mass", section on 'Assessing the risk of malignancy'.)
CANDIDATES — Candidates for OS include patients undergoing a pelvic operation for another indication (eg, hysterectomy for benign disease, permanent sterilization) and who have no plans for future pregnancy. If there are no indications for oophorectomy, the ovaries are conserved as oophorectomy is associated with adverse outcomes (eg, premature surgical menopause), including all-cause mortality and cardiovascular disease. (See "Elective oophorectomy or ovarian conservation at the time of hysterectomy".)
By contrast, patients at high risk for cancers of the fallopian tube, ovary, and peritoneum (eg, BRCA gene mutation, Lynch syndrome) are not candidates for OS and rather should undergo a risk-reducing bilateral salpingo-oophorectomy (rrBSO). While early salpingectomy with delayed oophorectomy has also been described in such patients [61], subsequent ovarian carcinomas (prior to the delayed oophorectomy) have been reported [62]. Thus, this practice remains investigational and studies are ongoing. (See "Risk-reducing salpingo-oophorectomy in patients at high risk of epithelial ovarian and fallopian tube cancer" and "Cancer risks and management of BRCA1/2 carriers without cancer", section on 'Bilateral salpingo-oophorectomy'.)
COUNSELING — In our practice, we counsel patients at average risk of epithelial ovarian carcinoma (EOC) who are undergoing hysterectomy for benign indications or sterilization about the risks and benefits of OS and employ shared decision-making with the patient. This is consistent with the approach of expert groups including the Society of Gynecologic Oncologists of Canada, Society of Gynecologic Oncology, American College of Obstetricians and Gynecologists, Royal Australian and New Zealand College of Obstetricians and Gynaecologists, and German Society of Gynaecology and Obstetrics (Deutschen Gesellschaft für Gynäkologie und Geburtshilfe) [63-67].
In place of tubal ligation — For patients undergoing surgical sterilization, we discuss all options for sterilization, including complete salpingectomy, and communicate that sterilization by salpingectomy is not reversible. We share the available data regarding minimal added surgical time and risk of morbidity. (See 'Outcomes' below.)
We offer OS for permanent sterilization via laparoscopy or laparotomy, including at the time of cesarean birth; the timing of the sterilization procedure affects how it is performed. Postpartum sterilization is performed at the time of cesarean birth or via a mini-laparotomy. Patients who undergo interval sterilization (ie, not during a postpartum period) may have either a laparoscopic or mini-laparotomy procedure. (See "Overview of female permanent contraception", section on 'Timing and surgical approach'.)
Sterilization with complete salpingectomy cannot be reversed. Counseling for all patients undergoing sterilization should emphasize that it is a permanent procedure and that there is no possibility of a tubal reanastomosis.
Patients undergoing hysterectomy for benign indications — For most patients who undergo hysterectomy with ovarian conservation, we perform salpingectomy. For patients undergoing vaginal hysterectomy, removal of the tubes is feasible with a transvaginal approach or can be performed with laparoscopic assistance. We do not change the surgical route to be able to perform OS unless this is the strong preference of the patient. (See "Hysterectomy (benign indications): Selection of surgical route", section on 'Prophylactic oophorectomy or salpingectomy'.)
Patients undergoing other abdominal surgery — While OS at the time of other abdominal procedures (eg, cholecystectomy) has been described, it is not routinely performed, likely due to lack of physician and patient awareness. However, when such patients are offered OS, acceptance rates are high. In a prospective study including patients undergoing elective laparoscopic cholecystectomy, the acceptance rate of concurrent OS was approximately 60 percent [68]. Of the 105 patients in which both procedures were planned, salpingectomy was successfully completed in 93 percent of patients; seven patients (6.7 percent) did not have the procedure performed due to poor visibility or pelvic adhesions. (See 'Perioperative outcomes' below.)
PROCEDURE
The goal of OS is the removal of at least the distal one-third (fimbria and infundibulum, portion of ampulla) of both fallopian tubes (figure 1) as this is the origin of the majority of cancers and preinvasive lesions in both the general population and BRCA1 and BRCA2 mutation carriers (see 'Role of the fallopian tube in carcinogenesis' above). Where possible, the entire extrauterine portion of the tube is removed.
This procedure can be accomplished using any surgical route (open, laparoscopic, robotic, or vaginal) and is described in detail separately:
●Open or laparoscopic hysterectomy – (See "Hysterectomy: Abdominal (open) route", section on 'Salpingectomy with ovarian conservation' and "Hysterectomy: Laparoscopic", section on 'Adnexa'.)
●Vaginal hysterectomy – (See "Hysterectomy: Vaginal", section on 'Adnexal evaluation and surgery'.)
●Surgical sterilization – (See "Postpartum permanent contraception: Procedures", section on 'Surgical approach' and "Postpartum permanent contraception: Procedures", section on 'Technique' and "Female interval permanent contraception: Procedures", section on 'Procedure'.)
When laparoscopic salpingectomy is performed, it is not necessary to place normal-appearing fallopian tubes from a patient at average risk of ovarian cancer in a containment bag for removal.
OUTCOMES
Perioperative outcomes
●Operative time – OS does not appear to substantively increase operative time [69-74]. In a population-based study in British Columbia including over 12,000 patients undergoing hysterectomy with or without bilateral salpingectomy, salpingectomy added an average of 16 minutes to the total operative time (133 versus 117 minutes [mean]) [75]. Similarly, for the almost 15,000 patients undergoing sterilization with either tubal ligation or complete salpingectomy, salpingectomy added an average of 10 minutes to the total operative time (71 versus 61 minutes [mean]). By contrast, in a subsequent cohort study including 4183 patients undergoing laparoscopic hysterectomy with or without salpingectomy, total operative time was reduced by five minutes in the salpingectomy group (154 versus 147 minutes [median]) [76]. In at least one study, salpingectomy at the time of cesarean birth was performed in approximately five minutes by experienced surgeons using the mesosalpinx isolation salpingectomy technique [77].
●Blood loss – OS also does not appear to substantively increase blood loss, as assessed through estimated blood loss, change in hemoglobin levels, and need for transfusion. In the large cohort study mentioned above, while patients undergoing hysterectomy (any route) with salpingectomy compared with hysterectomy alone had lower estimated blood loss (100 versus 150 mL [median]), this may have been due to lower blood loss in laparoscopic procedures or selection of less complicated cases for salpingectomy [76].
●Length of hospital stay – Length of hospital stay appears to be similar [78] or even reduced [69,72,75,76] for patients undergoing OS compared with hysterectomy alone.
●Perioperative complications – Perioperative complications also appear to be similar. In a large retrospective study including over 49,000 patients undergoing hysterectomy with or without salpingectomy or sterilization with tubal ligation or complete salpingectomy, rates of minor complications (eg, infection, hospital visits, laboratory tests ordered, imaging required) two weeks after hospital discharge were similar between groups [79]. However, more patients in the OS group filled a prescription for an analgesic during this time.
In a systematic review including seven randomized trials (350 patients) undergoing hysterectomy with or without OS, the number of surgery-related adverse events was too low to detect any difference [80]. To our knowledge, no studies have reported an increase in perioperative complications with OS as compared with hysterectomy alone or tubal ligation.
Ovarian cancer risk reduction — Complete salpingectomy is associated with a decreased risk of developing epithelial ovarian carcinoma (EOC) [81]. In a meta-analysis including three studies evaluating the impact of bilateral salpingectomy on EOC prevention over an 18- to 36-year (mean) follow-up period, patients with a history of prophylactic bilateral salpingectomy (3509 patients) versus no salpingectomy (5,655,702 patients) had an almost 50 percent lower risk of developing EOC (odds ratio 0.51, 95% CI 0.35-0.75) when results were adjusted for study size [82]. The absolute rates of EOC were similarly low in both groups (0.8 and 0.7 percent, respectively).
In a subsequent cohort study including 57,969 patients (mean age 38.2 to 40.2 years) comparing patients undergoing OS (45 percent of patients) with those undergoing hysterectomy or tubal ligation alone, OS was associated with a lower rate of serous (0 versus 15 patients) and epithelial (≤5 versus 21 patients) cancers during the 1.6 to 8.7 years of follow-up [83]. This was also lower than the age-adjusted expected rate of serous (5.27) and epithelial (8.68) cancers. As the observed and expected numbers of breast and colorectal cancers were similar, the difference in observed and expected ovarian cancers were likely not driven by differences between the groups.
In the systematic review of randomized trials discussed above (see 'Perioperative outcomes' above), none of the included studies specifically reported on the incidence of ovarian carcinoma after hysterectomy with or without OS [80].
Assessment of the effectiveness of OS for prevention of EOC is ongoing and requires that enough patients undergo the procedure for the purpose of primary ovarian cancer prevention and that these patients have enough follow-up time to develop ovarian cancers below the expected rate. It will likely take longer to demonstrate an impact for the cohort of patients who undergo salpingectomy for sterilization purposes, as the average age of salpingectomy for sterilization is 36.3 years [84], more than 20 years younger than the average age of diagnosis for nongenetic ovarian cancer [85]. As such, the impact of salpingectomy in ovarian cancer prevention and on histologic distribution of ovarian cancers will be the focus of the ongoing long-term study in British Columbia.
Ovarian function — It is uncertain whether salpingectomy impacts ovarian blood supply and hormonal function (eg, ovarian reserve, age of menopause). While hysterectomy is known to be associated with earlier menopause, this effect is not well understood. (See "Hysterectomy (benign indications): Patient-important issues and surgical complications", section on 'Decreased ovarian function or earlier menopause'.)
Some data suggest that tubal ligation [86-91] and bilateral salpingectomy [92,93] decrease ovarian reserve. For example, in a retrospective study including 6892 patients, those undergoing hysterectomy with or without bilateral salpingectomy had an increased risk of menopausal symptoms one year after surgery (31 versus 24 percent, adjusted relative risk 1.33, 95% CI 1.04-1.69) [94].
However, other data do not show an impact on ovarian reserve [74,95,96]. In the systematic review of randomized trials discussed above (see 'Perioperative outcomes' above), patients undergoing hysterectomy with or without OS had similar onset of menopause [80]. While mean postoperative anti-müllerian hormone (AMH) levels were lower in the OS group (1.89 to 0.01 pmol/L lower), this corresponds to the natural decline of AMH concentration of approximately 6 to 20 months, depending on age. Similarly, a large population-based retrospective cohort study including over 41,000 patients <50 years who underwent either OS with hysterectomy (compared with hysterectomy alone) or OS for sterilization (compared with tubal ligation) and followed for ≥5 years reported no evidence of an earlier age of onset of menopause among those undergoing OS compared with the relevant control groups (hysterectomy alone or tubal ligation) [84].
UTILIZATION — There has been an increased global acceptance of OS since its introduction as a potential ovarian cancer risk reduction strategy in 2010. While Canada was the first country to recommend consideration of OS during benign gynecologic surgery, by 2018 there were ten countries (Canada, Finland, United States, Great Britain, Australia, New Zealand, Denmark, Turkey, Austria, Japan) with International Federation of Obstetrics and Gynecology (FIGO) statements supporting OS [97]. In addition, four countries (Germany, Sweden, Norway, France) included ambivalent statements that addressed the subject but did not recommend for or against the procedure.
Utilization of the procedure is therefore increasing [75,98-103]. In a retrospective population-based cohort study in the United States including over one million patients undergoing hysterectomy for benign indications, rates of OS increased from 2.4 to 5.7 percent (between 2001 and 2010) to 58.4 percent by 2015; the rapid increase occurred after publication of data implicating the fallopian tubes in the pathogenesis of ovarian cancer [102]. In the large retrospective study of a large health care system discussed above (see 'Perioperative outcomes' above), higher rates (73 percent in 2014) were reported and salpingectomy was more common during laparoscopic hysterectomy compared with other routes [76]. Physicians reported the most important barriers to performing OS included: difficulty in accessing the fallopian tube, concern for increased complications, forgetting to address this issue preoperatively, and limited evidence to support its use.
SUMMARY AND RECOMMENDATIONS
●Definition – Opportunistic salpingectomy (OS) is the removal of the fallopian tubes for primary prevention of epithelial carcinoma of the fallopian tube, ovary, or peritoneum in average-risk patients undergoing pelvic surgery for another indication. By contrast, risk-reducing bilateral salpingo-oophorectomy (rrBSO) is a procedure performed in patients at high risk for these cancers. (See 'Introduction' above.)
●Rationale for performing this procedure
•Epithelial carcinoma of the ovary, fallopian tube, and peritoneum are considered a single entity and referred to collectively as epithelial ovarian carcinoma (EOC). While historically the ovaries were regarded as the most common primary sites of these cancers, data suggest that the majority of these cancers actually arise from the epithelium of the distal fallopian tube. (See 'Role of the fallopian tube in carcinogenesis' above.)
•Tubal ligation has consistently been shown to decrease the risk of developing EOC, providing additional support for the role of the fallopian tube in ovarian carcinoma pathogenesis. (See 'Efficacy of tubal ligation in cancer reduction' above.)
•In general, EOC presents at an advanced stage and has a poor prognosis (table 1). There are also no effective screening methods for these cancers. Thus, OS was proposed to reduce the risk of developing these cancers. (See 'Other' above.)
●Candidates – OS is appropriate for patients of any age who have no plans for future pregnancy. Patients at high risk for EOC (eg, BRCA gene mutation, Lynch syndrome) are not candidates for OS and rather should undergo a rrBSO. (See 'Candidates' above.)
●Counseling – The most common eligible procedures are hysterectomy for benign indications and sterilization. (See 'Counseling' above.)
•For most patients who undergo hysterectomy with ovarian conservation, we suggest performing bilateral salpingectomy (Grade 2C). For patients undergoing vaginal hysterectomy, removal of the tubes is feasible with a transvaginal approach or can be performed with laparoscopic assistance. We do not change the surgical route to be able to perform OS unless this is the strong preference of the patient.
•For patients undergoing surgical sterilization, we discuss all options for sterilization, including complete salpingectomy, and communicate that sterilization by salpingectomy is not reversible. We share the available data regarding minimal added surgical time and risk of morbidity. We offer OS for permanent sterilization via laparoscopy or laparotomy, and at the time of cesarean birth.
●Outcomes – The risks of salpingectomy appear to be minimal. Removal of the tube appears to add little to no time to the duration of hysterectomy or sterilization and appears to have no effect on morbidity. The impact of salpingectomy on ovarian function remains uncertain. (See 'Outcomes' above.)
ACKNOWLEDGMENT — The UpToDate editorial staff acknowledges Dianne M Miller, MD, FRCSC, who contributed to earlier versions of this topic review.
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