Ovarian cancer is the leading cause of mortality from gynecologic malignancy with more than 14,000 deaths from ovarian cancer in the United States estimated in 2015.1 Serous epithelial ovarian carcinoma accounts for the majority of deaths from ovarian cancer with three fourths of diagnoses occurring at advanced stages when prognosis is poor. Interventions that reduce ovarian cancer risk are especially important given the lack of effective screening strategies and the fact that mortality rates from the disease have not changed significantly over the past several decades.2 Over the past 10 years, evidence from serous tubal intraepithelial carcinoma lesions detected in BRCA carriers undergoing risk-reducing salpingo-oophorectomies as well as molecular studies of serous tubal intraepithelial carcinoma lesions has suggested that a majority of serous epithelial ovarian cancer likely arises in the fallopian tube, particularly the fimbria.3–11 Although it is known that tubal ligation decreases ovarian cancer risk, it is theorized that complete removal of the fallopian tubes could prevent more cases of serous ovarian cancer.12 The ability to prevent epithelial ovarian cancer by removal of the fallopian tubes at the time of elective pelvic surgery is an attractive risk-reducing strategy and would still allow preservation of ovarian hormone production.
The practice of opportunistic salpingectomy was supported by the Society of Gynecologic Oncology of Canada in 2011, with subsequent increases in the procedure demonstrated after physician education interventions. An educational video was sent to every obstetrician–gynecologist (ob-gyn) in British Columbia recommending a change in general gynecologic practice to include opportunistic salpingectomy at the time of gynecologic surgeries and resulted in a significant increase in uptake of salpingectomy from 5% to 35%.13 In May 2013, Kaiser Permanente Northern California published a practice resource describing theoretical benefits and techniques of performing salpingectomy, recommending it be discussed with all women undergoing benign pelvic surgery. It was widely distributed to all the ob-gyns practicing in Kaiser Permanente Northern California with online access to the educational material provided (Appendix 1, available online at http://links.lww.com/AOG/A829). Later that year, the Society of Gynecologic Oncology published a statement supporting consideration of opportunistic salpingectomy at the time of benign gynecologic surgery.14
The objective of this study was to assess the rate of salpingectomy at the time of hysterectomy without oophorectomy during time periods before and after the publication of the Kaiser Permanente Northern California practice resource. It was hypothesized that there would be an increase in salpingectomy over time. We additionally sought to assess physicians' attitudes toward the practice, perceived barriers to performing salpingectomy, and experiences with complications.
MATERIALS AND METHODS
A retrospective cohort study with chart review using the Kaiser Permanente Northern California electronic medical record was performed. Kaiser Permanente Northern California is a diverse integrated health care delivery system with more than 3.6 million members. An initial abstraction from the electronic medical record was performed using procedure codes to identify all women 18 years of age or older who underwent hysterectomy or hysterectomy with salpingectomy from June 2011 to May 2014. Hysterectomy with salpingectomy was defined as having the bilateral procedure coded. Women were excluded if they underwent a procedure that involved any oophorectomy, if they had a diagnosis of any cancer, or if they were BRCA1 or BRCA2 mutation carriers. Information on patient age, race, neighborhood poverty, body mass index (BMI, calculated as weight (kg)/[height (m)]2), prior tubal ligation, and surgical factors such as route of hysterectomy, operating time, postoperative length of stay, and estimated blood loss were also abstracted from the medical record. Operating room time was from incision to close and postoperative length of stay was from the time the patient left the operating room until the time of discharge. A chart review was performed on a random sample of 1% (120) of all excluded and included cases for data validation and to estimate the accuracy of extracted data.
All ob-gyns in Kaiser Permanente Northern California were sent a link to an anonymous electronic survey by e-mail in January 2015, approximately 20 months after the Kaiser Permanente Northern California salpingectomy resource had been circulated. Health care providers then received two e-mail reminders to complete the survey over the next 2-month period. The survey included questions on clinical demographics, scope of practice, knowledge of salpingectomy complications and benefits, adoption of salpingectomy, and barriers to implementation. The full survey is included in Appendix 2, available online at http://links.lww.com/AOG/A830. As a result of a relatively low response rate, the physician survey results are reported in a descriptive manner.
Rates of salpingectomy at the time of hysterectomy for each year interval in the study (June 2011 to May 2012, June 2012 to May 2013, and June 2013 to May 2014) and before and after the distribution of the Kaiser Permanente Northern California practice resource were compared using χ2 tests. A bivariate analysis was performed to identify demographic and clinical factors associated with performance of salpingectomy. Continuous variables were described with medians and compared with the Wilcoxon-Mann-Whitney test. Chi square tests were used for categorical variables. All tests were two-tailed with a P<.05 considered statistically significant and all analyses were performed using SAS 9.3. The Kaiser Foundation Research Institute's institutional review board approved this study with waiver of consent.
From June 2011 to May 2014, a total of 12,143 hysterectomies were performed for benign disease with 7,498 without oophorectomy meeting our inclusion criteria. The majority of hysterectomies, 55.4% (4,154/7,498), were performed without salpingectomy. However, there was a statistically significant increase in the rate of salpingectomy over time with a rate of 14.7% (95% confidence interval [CI] 13.3–16.1) from June 2011 to May of 2012, 44.6% (95% CI 42.6–46.5) from June 2012 to May 2013, and 72.7% (95% CI 71.0–74.4) from June 2013 to May 2014 (P<.001) (Fig. 1). Comparing predistribution and postdistribution of the Kaiser Permanente Northern California provider resource, the increase in the uptake of salpingectomy is similar, from 29.8% (95% CI 28.6–31.1) in the study period from June 2011 to May 2013 before the practice bulletin to 72.7% (95% CI 71.0–74.4) in the period May 2013 to study end, May 2014 postpractice bulletin. Chart review revealed that 92.7% (95% CI 85.3–95.4%) were accurate with regard to inclusion and exclusion criteria and 95% (95% CI 86.3–98.3%) were accurate with regard to performance of salpingectomy.
The median age at the time of hysterectomy was 45.0 years with women in the hysterectomy alone cohort older than women in the hysterectomy with salpingectomy cohort (46.0 compared with 44.0 years, P<.001). Opportunistic salpingectomy was statistically associated with race (P<.001), BMI (P=.01), and surgical route (P<.001). Of clinical significance, laparoscopic hysterectomies were more likely to be performed with salpingectomy (60.5%), whereas abdominal and vaginal hysterectomies were less likely to be performed with salpingectomy (24.6% and 16.5%, respectively). There was some geographic variation in the rate of opportunistic salpingectomy, ranging from 42.0% to 48.0% among the six Kaiser Permanente Northern California service areas (P=.02). There was no significant association between opportunistic salpingectomy and socioeconomic status or history of tubal ligation (Table 1).
Median estimated blood loss, not stratified by route of procedure, was lower in the salpingectomy group compared with hysterectomy alone (100 compared with 150 mL, P<.001) (Table 2). Operating time was significantly shorter in the salpingectomy compared with the hysterectomy alone group in those undergoing laparoscopic procedures (147 compared with 154 minutes, P=.002). There was no difference in operating time by performance of salpingectomy for vaginal or abdominal hysterectomies. There was also a significantly shorter length of stay in the salpingectomy group for patients who had undergone a laparoscopic (4.0 compared with 4.9 hours, P<.001) or vaginal procedure (19.4 compared with 23.8 hours, P<.001), but not an abdominal hysterectomy (Table 2).
There was a 46% (249/543) response rate to the physician survey. The majority of physicians were female (76%), had practiced for 10–20 years (36%), and were specialist (“generalist”) practitioners (89%). Of the physicians who perform hysterectomies, 86% (193/223) reported having incorporated salpingectomy into their practice. Physicians in practice for more than 20 years appeared less likely to perform salpingectomy than those in practice for less than 20 years. There was no apparent difference in gender or type of practice in terms of whether physicians reported performing salpingectomy.
When physicians were asked “At the time of hysterectomy, what was the most important barrier you see to performing salpingectomy?” most physicians reported no barriers (54%). The next most common responses were “difficulty in accessing the tube” (36%) and “increased complications” (3%) (Fig. 2).
The majority of physicians reported no increase in complications with addition of salpingectomy at the time of hysterectomy (91%). Only 6.8% of physicians reported experiencing increased operating room time and only 2.1% reported increased estimated blood loss with the addition of salpingectomy at the time of hysterectomy.
The practice of opportunistic salpingectomy at the time of elective hysterectomy significantly increased over each year of the study period from June 2011 to May 2014. By the end of the study, a remarkable 72.7% of hysterectomies were being performed with salpingectomy, mostly during laparoscopic procedures. This is higher than previously reported rates derived from large databases in the U.S. population.15,16
This study adds to the literature by combining a large cohort in the United States with a survey of health care providers serving the same patient population. Notably, the survey had a low response rate and is reported descriptively only to identify some issues for future, robust evaluation. Overall, there was no clinical difference in surgical time, length of stay, or estimated blood loss, similar to the findings of McAlpine et al,13 who demonstrated an average increase of 16 minutes of operating room time with the addition of salpingectomy to hysterectomy and no difference in transfusions. Although our estimated blood loss was lower in the salpingectomy group, this was not stratified by route and may be the result of the higher proportion of laparoscopic hysterectomies. In the McAlpine series of more than 40,000 Canadian women, they also found no increase in length of stay or readmission when salpingectomy was added to hysterectomy.13 Other studies reporting outcomes and complications of salpingectomy in premenopausal women undergoing hysterectomy further support the safety of the procedure with no significant differences in operating room time, estimated blood loss, or other intraoperative complications.17,18
There have been concerns that any risks of performing this additional surgical procedure might not be worth the theoretical benefits. However, in a small report from the United States, excisional tubal ligation procedures (salpingectomy, fimbriectomy, or partial salpingectomy) were associated with greater ovarian cancer risk reduction when compared with nonexcisional procedures.19 In a larger study from Denmark, Madsen et al20 also demonstrated that bilateral salpingectomy was associated with a decreased risk of epithelial ovarian cancer compared with tubal ligation (odds ratio 0.58 compared with 0.87). This was further supported by a Swedish cohort study demonstrating greater ovarian cancer risk reduction from salpingectomy compared with tubal ligation with twice the risk reduction seen from a bilateral compared with a unilateral procedure.21 Although these were retrospective studies, they are the first to directly link salpingectomy with decreased risk of ovarian cancer and show a greater benefit than for tubal ligation alone. Kwon et al22 performed Markov Monte Carlo simulation modeling to evaluate effectiveness and cost of opportunistic salpingectomy for ovarian cancer prevention and demonstrated that hysterectomy with salpingectomy was less costly and more effective than either hysterectomy alone or hysterectomy plus bilateral salpingo-oophorectomy. Understanding the true benefit of the procedure in terms of ovarian cancer risk reduction will involve prolonged follow-up of current cohorts undergoing the procedure.
We also demonstrated high levels of acceptance of the practice of opportunistic salpingectomy among our health care providers who responded to the survey. There is no financial benefit to health care providers for choosing to perform salpingectomy. Interpretation of our survey results is limited by a less than 50% response rate, although the responses do provide a descriptive example of health care providers' perceptions and experiences. Prior surveys of physicians have demonstrated greater concerns to performing the procedure. In a 2012 survey of 234 U.S. ob-gyns by Gill and Mills, self-reported rates of practicing opportunistic salpingectomy were 54%, lower than our rate of 86%. Interestingly, similar reasons for not performing salpingectomy with hysterectomy were listed, but at much higher rates, including no perceived benefit (69.4%), increased operative time (40%), and increased risk of intraoperative complications (34%).23 In a more current survey of 192 Canadian physicians (response rate 25%), Reade et al24 showed that many physicians still felt there were concerns with performing the procedure including increased complications (52%), increased operating time (43%), and increased time for patient counseling (28%). In contrast, the majority of physicians in our study identified no barriers to performing salpingectomy and 91% reported no increase in complications. The most common barrier identified by our physicians was technical difficulty in accessing the tube, as reflected by the lower rate of salpingectomy seen with vaginal hysterectomies.
The main strengths of this study include using a large electronic database to generate a robust data set, validated with chart review, to analyze the uptake of performing risk-reducing salpingectomy over a discrete time period. The study period encompasses a timeframe over which new statements of support for salpingectomy from national organizations were published, allowing us to examine an appropriate time period in which to expect change.
Limitations include the low response rate of 46%, which introduces risk of selection bias, with the potential for health care providers who perform salpingectomy more likely to complete the survey.
Objective data on procedures performed as well as complications were reported for contrast to the survey data and to attempt to account for this potential selection bias. Although health care providers may be discussing salpingectomy, this study does not evaluate for other potential barriers such as patient acceptance, which should be evaluated in the future. In addition, we did not control for possible confounders that could be related to increased operating room time or estimated blood loss such as number of prior surgeries, BMI, route, or endometriosis. There are limitations in using coded data to define procedures with the potential for misclassification. We also could not examine all prior surgical history so women with a prior removal of tubes would have been included in the hysterectomy alone group. Although this likely represents a small number of patients, it would make our rates of salpingectomy appear lower than in actuality. The change in salpingectomy rate before and after our intervention was not dramatically larger than the increases seen from year to year. This makes it difficult to tease out the effect of our educational intervention compared with uptake from other factors that change over time such as recommendations from professional organizations.
We report a large increase in rate of salpingectomy from 14.7% to 72.7% over the course of our study during which an educational intervention occurred with the intention to change clinical practice. In addition, we add to the literature on the safety and feasibility of performance of opportunistic salpingectomy with no clinical difference in operating time, length of stay, or blood loss. The full benefits of the practice have yet to be realized and an educational intervention may be a successful model for accelerating this practice change in the context of the national and international discussions of the procedure.
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