Racial and ethnic differences in the adoption of opportunistic salpingectomy for ovarian cancer prevention in the United States.

Between 2011 and 2018, we identified 247,787 benign hysterectomies and 403,118 surgical sterilizations. Overall, the proportion of hysterectomies involving OS increased from 6.3% in 2011 to 59.7% in 2018 ( Figure 2A ) and the proportion of sterilizations involving OS increased from 0.7% in 2011 to 19.4% in 2018 ( Figure 2B ). The adoption of OS increased across all race and ethnicity groups. The proportion of OS during hysterectomy increased from 6.1% to 56.8%, 5.4% to 63.4%, 7.7% to 62.4%, and 7.8% to 64.5% and the proportion of OS for sterilization increased from 0.8% to 22.8%, 0.7% to 14.5%, 0.5% to 15.1%, and 0.7% to 18.2% from 2011 to 2018 in NHW, NHB, Hispanic, and NHO women, respectively. A total of 164,995 women underwent hysterectomy alone and 82,792 women underwent hysterectomy and OS ( Table 1 ). Most women were NHW (hysterectomy: 60.3%; hysterectomy and OS: 60.3%). About 19.4%, 12.0%, 8.3% of women undergoing hysterectomy and 18.8%, 12.2%, 8.7% of women undergoing hysterectomy and OS were NHB, Hispanic, and NHO, respectively. Women undergoing hysterectomy (mean age, NHW: 40.0 years, NHB: 40.9 years, Hispanic: 40.7 years, NHO: 40.9 years) were younger than those undergoing hysterectomy and OS (mean age, NHW: 40.5 years, NHB: 41.6 years, Hispanic: 41.3 years, NHO: 41.9 years), with minimal differences by race and ethnicity. Significant differences with respect to surgery type and race and ethnicity were observed for the year of surgery, marital status, type of insurance, number of comorbidities, hysterectomy route, indications for hysterectomy, hospital location, hospital region, hospital teaching status, place of service, annualized hospital volume, and hospital proportion of Medicaid and uninsured patients. A total of 379,720 women underwent tubal ligation and 23,398 women underwent OS for sterilization ( Table 2 ). Most women were NHW (tubal ligation: 53.6%, OS: 64.7%). About 15.0%, 21.8%, 9.6% of women undergoing tubal ligation and 10.8%, 16.7%, 7.8% of women undergoing OS for sterilization were NHB, Hispanic, and NHO, respectively. Women undergoing tubal ligation (mean age, NHW: 31.9 years, NHB: 31.0 years, Hispanic: 32.3 years, NHO: 32.9 years) were younger than women undergoing OS for sterilization (mean age, NHW: 34.2 years, NHB: 33.7 years, Hispanic: 33.5 years, NHO: 35.1 years), with minimal differences by race and ethnicity. Significant differences with respect to surgery type and race and ethnicity were observed for the year of surgery, type of insurance, number of comorbidities, type of sterilization, hospital location, hospital region, hospital teaching status, place of service, annualized hospital volume, and hospital proportion of Medicaid and uninsured patients. NHB (RR: 0.94, 95% CI: 0.92–0.97), Hispanic (RR: 0.98, 95% CI: 0.95–1.00), and NHO women (RR: 0.93, 95% CI: 0.90–0.96) were less likely to undergo hysterectomy and OS than NHW women ( Table 3 ). A significant interaction between race and ethnicity and year of surgery was observed in NHB compared to NHW women ( P <0.001), with a reduction in differences in hysterectomy and OS use after national guideline release supporting OS use (RR 2011–2013 : 0.80, 95% CI: 0.73–0.88; RR 2014–2018 : 0.98, 95% CI: 0.95–1.01). No interaction with the year of surgery was observed in Hispanic and NHO women. NHB women were also less likely to undergo OS for sterilization than NHW women (RR: 0.91, 95% CI: 0.88–0.95), with no difference by year of surgery ( P = 0.62). There was no difference in OS for sterilization use between Hispanic and NHW women (RR: 1.00, 95% CI: 0.94–1.06) and NHO and NHW women (RR: 0.99, 95% CI: 0.85–1.15). Results remained unchanged when a washout period was imposed to allow time for national guideline implementation ( Supplemental Table 2 ) and when the year of surgery cut points were changed to reflect the American College of Obstetricians and Gynecologists committee opinion supporting OS use ( Supplemental Table 3 ). Racial and ethnic differences in hysterectomy and OS use were observed for all hysterectomy routes ( Supplemental Table 4 ). In analyses by age at surgery, differences in hysterectomy and OS use and OS for sterilization use between NHB and NHW women and differences in hysterectomy and OS use between NHO and NHW women were observed in all age groups. Differences in hysterectomy and OS use between Hispanic and NHW women were restricted to those 18–34 years old at the time of surgery ( Supplemental Table 5 ). Women with missing race and ethnicity data were more likely to seek care in the Midwest and West and in low volume hospitals than those without missing data. There were no differences in sociodemographic, clinical, and procedural characteristics between women with and without missing race and ethnicity data ( Supplemental Table 6 ). The results of the multiple imputation analysis were similar in magnitude and direction to the complete case analysis ( Supplemental Table 7 ).

In this national sample of women undergoing hysterectomy with ovarian conservation or surgical sterilization from 2011 to 2018, NHB, Hispanic, and NHO women were less likely to undergo OS than NHW women. Although the release of national guidelines supporting OS use reduced differences in hysterectomy and OS use between NHB and NHW women, differences in hysterectomy and OS use between NHO and NHW women and differences in OS for sterilization use between NHB and NHW women persisted after guideline release. The release of national guidelines had no impact on differences in hysterectomy and OS use between Hispanic and NHW women. Racial and ethnic differences in OS use were not fully explained by sociodemographic, clinical, procedural, hospital, and provider characteristics. To our knowledge, this is one of the first studies to examine racial and ethnic differences in OS adoption. Our study addresses a critical gap in the OS literature by utilizing a geographically diverse sample of inpatient and outpatient procedures with detailed information on patient-, provider-, and hospital-level factors to comprehensively characterize racial and ethnic differences in OS adoption. A prior study that used the National Inpatient Sample found that NHB (odds ratio [OR]: 1.04, 95% CI: 1.02–1.06), Hispanic (OR: 1.11, 95% CI: 1.09–1.14), Asian (OR: 1.20, 95% CI: 1.05–1.14), and other women (OR: 1.08, 95% CI: 1.04–1.12) were more likely to undergo hysterectomy and OS than NHW women. 11 However, this study was limited to inpatient settings and may have underestimated the number of hysterectomy and OS procedures performed in NHW women. Additionally, about 19% of women included in the study had missing information on race and ethnicity. Most hysterectomy and OS procedures in our study were performed in outpatient settings (61.1% overall), with NHW women (69.5%) more likely to undergo the procedure in outpatient settings compared to all other race and ethnicity groups (NHB: 45.2%, Hispanic: 45.8%, other: 58.6%). Furthermore, our results were robust and did not change when missing data on race and ethnicity were imputed. The reasons for the racial and ethnic differences in OS use observed in this study are likely multifactorial. Research has shown that Black patients are less willing to accept novel medical interventions, 35 which may extend to novel gynecologic surgeries such as OS. The legacy of medical experimentation in reproductive-aged Black women and forced sterilization among immigrant Hispanic women 36 – 40 may limit trust in novel gynecologic surgeries in these communities. Other factors such as provider bias, patient knowledge and preferences, levels of participation in healthcare interactions and decisions, and differences in the quality of care at facilities attended by different racial and ethnic groups may also have contributed to the differential adoption of OS observed in this study. 41 From a clinical standpoint, interventions to promote equitable OS uptake are needed to reduce racial differences in this potentially life-saving preventive procedure. 4 – 6 Since OS is becoming more common in clinical practice, even minor differences in OS use by race and ethnicity may lead to emerging disparities in population-level ovarian cancer incidence in the future. Additional data are needed to understand when and how clinicians approach discussions about OS for ovarian cancer prevention in different race and ethnicity groups. Future studies should also examine the impact of systemic factors, such as implicit race and social class bias, and how they may impact provider enthusiasm and surgical decision-making. More research is also needed to better understand patient- provider-, and hospital-level factors influencing OS uptake among diverse women, including whether observed patterns reflect racial differences in access to healthcare systems and/or clinicians who are low or high adopters of OS. These data will be critical in providing targets for future interventions to ensure that the benefits of OS for ovarian cancer prevention are equitably distributed. Our study has several limitations. First, we could not capture individual patient and physician perceptions and attitudes, which likely influenced OS uptake. Second, we lacked information on patient-level factors, such as prior surgical history and family history of and genetic susceptibility to ovarian cancer that may have influenced surgical decision-making. Third, Asian, Pacific Islander, American Indian, and Alaska Native women, and those reporting multiple races were aggregated within the Premier database into the non-Hispanic other race category to protect patient privacy. Therefore, we could not assess OS use in these subgroups. Fourth, although the Premier database is broadly representative of U.S. hospitals and health systems, it includes a relatively high proportion of small to mid-size non-teaching hospitals in urban locations; therefore, our results may not be generalizable to other settings and should be interpreted with caution. Finally, our analysis is limited by the nature of claims data, which may involve errors in coding and incomplete documentation that could lead to the misclassification of covariates. ICD/CPT codes for OS have not been validated; therefore, we developed a minimally sufficient set of codes to reduce misclassification. The potential for misclassification of OS to be differential by race and ethnicity is likely low. Despite these limitations, our study examined a contemporary and geographically diverse population-based cohort of women undergoing OS in both inpatient and outpatient settings. Prior studies have used databases limited to inpatient settings, 9 – 11 providing an incomplete view of OS adoption. We also controlled for patient-, provider-, and hospital-level factors that are associated with the uptake of gynecologic surgeries. Another major strength of our study is that we focused on differences in OS adoption by race and ethnicity, which is not possible in many claims-based datasets and, to our knowledge, has not been comprehensively examined before. Our study offers new evidence to suggest that despite the rapid adoption of OS for ovarian cancer prevention in the U.S., NHB, Hispanic, and NHO women are less likely to undergo OS than NHW women. Racial differences in OS use persisted even after accounting for patient-, provider-, and hospital-level factors and after the release of national guidelines supporting OS use. Additional studies are needed to identify barriers to OS adoption in racial and ethnic minority women to inform interventions that promote equity in OS use.

We analyzed data from the Premier Perspective Healthcare Database, a de-identified, all-payer hospital administrative database with inpatient and outpatient services rendered at over 700 hospitals across the U.S. 25 Premier contains information on sociodemographic and clinical characteristics and provider and hospital-specific data, including all diagnoses and procedures. The study was deemed exempt by the Columbia University Institutional Review Board. Figure 1 shows the criteria used to identify the study population. Cancer-free women 18–50 years with an inpatient or outpatient claim for hysterectomy, tubal ligation, or bilateral salpingectomy between January 2011 to June 2018, were identified (n=1,142,913). Both elective and emergent surgeries were included. Women with a concomitant bilateral oophorectomy/salpingo-oophorectomy (n=225,974), those with hysterectomy codes without detail regarding the removal of additional adnexal structures (n=81,696), those undergoing tubal ligation or OS for indications other than sterilization (n=20,253), and those with unknown race and ethnicity were excluded (n=164,085). After exclusions, 650,905 women were included in the study population, 247,787 with benign hysterectomy procedures and 403,118 with surgical sterilization procedures. Women were classified into four distinct groups by surgery type: hysterectomy alone without OS (n=164,995), hysterectomy and OS (n=82,792), tubal ligation (n=379,720), and OS for sterilization (n=23,398). A set of International Classification of Diseases (ICD) procedure codes were utilized to classify inpatient surgeries and Current Procedural Terminology (CPT) codes were utilized to classify outpatient surgeries ( Supplemental Table 1 ). 14 Women with at least one code in Group 1 and none in Groups 2 or 3 were classified as hysterectomy alone without OS, those with at least one code in Groups 1 and 3 and none in Group 2 were classified as hysterectomy and OS, those with at least one code in Group 2 and none in Groups 1 or 3 were classified as tubal ligation, and those with at least one code in Group 3 and none in Groups 1 or 2 were classified as OS. Race and ethnicity were derived from the uniform medical billing form associated with the surgery claim. Race was classified as Black, White, other, or unknown, and ethnicity was classified as Hispanic, non-Hispanic, or unknown. A composite race and ethnicity variable was created and classified as non-Hispanic White (NHW), non-Hispanic Black (NHB), Hispanic any race, non-Hispanic other race (NHO), and unknown. Women with unknown race and/or ethnicity were not included in the analysis. Sociodemographic, clinical, procedural, hospital, and provider characteristics were ascertained for all women. Sociodemographic characteristics included age, year of surgery (2011–2013, 2014–2018), marital status (married, single, other, unknown), and insurance type (commercial, Medicare, Medicaid, uninsured, unknown). Clinical and procedural characteristics included comorbidities (0, 1, ≥2), type of sterilization (interval, postpartum), hysterectomy route (abdominal, laparoscopic, robotic-assisted, vaginal), and indications for hysterectomy (uterine fibroids, endometriosis, abnormal bleeding, benign neoplasms and cysts, pelvic organ prolapse). Comorbidities were ascertained using the Elixhauser comorbidity index, 26 , 27 and type of sterilization, hysterectomy route, and indications for hysterectomy were identified based on the ICD and CPT codes associated with the surgery claims ( Supplemental Table 1 ). Hospital and provider characteristics included location (rural, urban), region (Midwest, Northeast, South, West), teaching status (non-teaching, teaching), bed size (499), place of service (inpatient, outpatient), hospital volume (low [≤200 procedures/year], intermediate [201–403 procedures/year], high [≥404 procedures/year]), proportion of Medicaid and uninsured patients (low [≤33%], intermediate [34%–46%], high [≥46%]), and provider specialty (obstetrics and gynecology, gynecologic oncology, other). Hospital volume was determined by dividing the total number of women undergoing surgery at each hospital by the number of years each hospital contributed at least one surgery and categorized into tertiles. The proportion of Medicaid and uninsured patients was determined by dividing the number of Medicaid and uninsured women undergoing surgery at each hospital by the number of hospitals that contributed at least one Medicaid or uninsured patient and categorized into tertiles. Descriptive analyses by race and ethnicity and type of OS were conducted, and the proportion of benign hysterectomy and surgical sterilization procedures involving OS were plotted by race and ethnicity and year. Multivariable mixed-effects log-binomial regression models were used to examine the association between race and ethnicity and OS during hysterectomy (hysterectomy and OS vs. hysterectomy alone) and OS for sterilization (OS alone vs. tubal ligation). Models included a random intercept term for the hospital in which the surgery was performed to account for hospital-level clustering. All models were adjusted for sociodemographic characteristics (age, year, marital status, insurance type), clinical and procedural characteristics (comorbidities, type of sterilization, hysterectomy route, indications for hysterectomy), and hospital and provider characteristics (location, region, teaching status, bed size, place of service, hospital volume, proportion of Medicaid and uninsured patients, provider specialty).These covariates were selected based on clinical rationale and prior literature. 11 , 28 , 29 All models also included a multiplicative interaction term between race and ethnicity and year of surgery (2011–2013 [before guideline], 2014–2018 [after guideline]) to test if racial and ethnic differences in OS adoption changed after the release of national guidelines supporting OS use. The year cut point was based on the November 2013 release of the Society of Gynecologic Oncology clinical practice statement. 7 Results were reported as risk ratios (RR) and 95% confidence intervals (CI). Sensitivity analyses were conducted to test whether overall results changed by excluding 2014 from the analysis to allow time for guideline implementation and changing year of surgery cut points to the American College of Obstetricians and Gynecologists committee opinion supporting OS use (2011–2014 [before guideline], 2015–2018 [after guideline]). 8 For hysterectomy and OS, stratified analyses by hysterectomy route were performed as prior studies have shown that Black and Hispanic women are less likely to undergo minimally invasive hysterectomy and more likely to undergo abdominal hysterectomy. 17 , 18 Additional analyses by age at surgery (18–34, 35–44, 45–50 years) were also performed as rates of hysterectomy and surgical sterilization vary by age. 30 – 32 To further assess the sensitivity of our results, missing data on race and ethnicity (n=164,085) were imputed based on observed values, assuming the data were missing at random. A total of 10 datasets were imputed using the multivariate imputation by chained equations method, and the results were combined across imputations using standard methods. 33 , 34 All analyses were conducted in Stata, version 17.0 (Stata Corporation).

Accumulating evidence showing that high-grade serous ovarian cancer may originate in the fallopian tubes 1 – 3 has led to the emergence of opportunistic salpingectomy (OS), the removal of the fallopian tubes during benign gynecologic surgery, as a novel strategy for ovarian cancer prevention. Data from three observational studies suggest that OS is associated with a 42%–64% reduction in ovarian cancer risk. 4 – 6 In the U.S., both the American College of Obstetricians and Gynecologists and the Society of Gynecologic Oncology now recommend OS for ovarian cancer prevention in average-risk women at the time of a benign hysterectomy or in place of tubal ligation for sterilization. 7 , 8 Several studies have shown that clinicians in the U.S. have rapidly adopted OS. 9 – 11 The most recent study found that the proportion of OS during hysterectomy increased from 2.4% in 2001 to 58.4% in 2015. 11 However, these studies provide an incomplete picture of OS adoption and have limited generalizability because they were restricted to inpatient settings, which is not reflective of where most benign gynecologic surgeries are performed in the U.S. 12 , 13 A study examining OS adoption in a national sample of inpatient and outpatient procedures found that the proportion of OS during hysterectomy increased from 1% in 2010 to 32% in 2017 and the proportion of OS for sterilization increased from 1% in 2010 to 20% in 2017. 14 In this study, 23% of hysterectomy and OS and 80% of OS for sterilization were performed as outpatient procedures, underscoring the importance of including inpatient and outpatient data when assessing changing trends in gynecologic surgeries. To our knowledge, no studies have examined racial and ethnic differences in OS adoption. As with other medical innovations, surgical innovations in gynecology may be adopted differentially among racial and ethnic minorities, exacerbating disparities in quality of care. 15 , 16 Racial and ethnic differences in gynecologic surgical care are pervasive and have been well-documented. Prior studies have shown that Black, Hispanic, and Asian/Pacific Islander women are more likely to undergo open abdominal hysterectomies and less likely to undergo minimally invasive hysterectomies, 17 – 19 which are associated with fewer postoperative complications and a shorter hospital stay. 20 These differences in hysterectomy route persist even after accounting for insurance coverage, surgical indications, uterus size, body mass index, surgeon training and experience, hospital volume, and history of prior pelvic surgery. 17 – 19 Additionally, although Black and Hispanic women are more likely to rely on surgical sterilization for contraception than White women, 21 , 22 they are also more likely to experience barriers accessing postpartum surgical sterilization than White women. 23 These documented differences may also impede the dissemination of novel preventive surgeries such as OS. Furthermore, age-adjusted ovarian cancer incidence rates vary across race and ethnicity groups, with White women having the highest incidence (11.3 per 100,000), followed by Hispanic (10.3 per 100,000), Asian/Pacific Islander (9.4 per 100,000), and Black women (9.0 per 100,000). Although ovarian cancer incidence rates declined significantly between 2014 and 2018, the rate of decline has been greatest in White women (average annual percent change: −3.7%) than all other race and ethnicity groups (Hispanic: −0.9%, Black: −0.8%, Asian/Pacific Islander: −0.3%). 24 Given that OS has rapidly diffused into clinical practice, if its adoption is not equitable, racial and ethnic disparities in ovarian cancer incidence may emerge in the future. The objective of this study was to evaluate racial and ethnic differences in OS adoption among women undergoing benign hysterectomies or surgical sterilization in a large and geographically diverse sample of inpatient and outpatient procedures and assess the impact of national guidelines supporting OS use on these differences.