Background:

We investigated racial and ethnic disparities in treatment sequence [i.e., neoadjuvant chemotherapy (NACT) plus interval debulking surgery (IDS) versus primary debulking surgery (PDS) plus adjuvant chemotherapy] among patients with ovarian cancer and its contribution to disparities in mortality.

Methods:

Study included 37,566 women ages ≥18 years, diagnosed with stage III/IV ovarian cancer from the National Cancer Database (2004–2017). Logistic regression was used to compute ORs and 95% confidence intervals (CI) for racial and ethnic disparities in treatment sequence. Cox proportional hazards regression was used to estimate HRs and 95% CI for racial and ethnic disparities in all-cause mortality.

Results:

Non-Hispanic Black (NHB) and Asian women were more likely to receive NACT plus IDS relative to PDS plus adjuvant chemotherapy than non-Hispanic White (NHW) women (OR: 1.12; 95% CI: 1.02–1.22 and OR: 1.12; 95% CI: 0.99–1.28, respectively). Compared with NHW women, NHB women had increased hazard of all-cause mortality (HR: 1.14; 95% CI: 1.09–1.20), whereas Asian and Hispanic women had a lower hazard of all-cause mortality (HR: 0.81; 95% CI: 0.74–0.88 and HR: 0.83; 95% CI: 0.77–0.88, respectively), which did not change after accounting for treatment sequence.

Conclusions:

NHB women were more likely to receive NACT plus IDS and experience a higher all-cause mortality rates than NHW women.

Impact:

Differences in treatment sequence did not explain racial disparities in all-cause mortality. Further evaluation of racial and ethnic differences in treatment and survival in a cohort of patients with detailed treatment information is warranted.

Ovarian cancer is the fifth leading cause of cancer-related mortality among women and the most lethal gynecologic malignancy in the United States (1). Because of the lack of early signs and symptoms and cost-effective screening tests, more than 70% of patients with ovarian cancer are diagnosed at an advanced stage contributing to a dismal overall 5-year relative survival of approximately 40% (2–4).

Studies have consistently reported evidence for racial and ethnic disparities in ovarian cancer treatment and survival, whereby non-Hispanic Black (NHB) women are more likely to die from their disease compared with non-Hispanic White (NHW) women (5–7). NHB women are more likely to be diagnosed with a later stage disease (8), fail to receive upfront surgery (9), have more residual disease after surgery, have treatment delays and early discontinuation, and receive chemotherapy at lower relative dose intensity than NHW women (5, 10–12). The causes for these disparities are likely multifactorial—some factors implicated include stage and grade at diagnosis, adherence to treatment, and access to care (5, 7). Racial and ethnic disparities in treatment patterns and overall survival (OS) for Asian and Hispanic women have received less attention. The few studies that evaluated survival disparities reported similar or better OS for Asian and Hispanic women compared with NHW women, yet further evidence is needed (13–16).

The treatment paradigm for ovarian cancer has changed in recent years. In 2010, results from a randomized clinical trial demonstrated noninferior survival for patients with ovarian cancer with advanced-stage disease treated with neoadjuvant chemotherapy (NACT; ref. 17). Following these results, use of NACT increased dramatically from approximately 8.6% in 2004 to 23% in 2013 (18–20). Primary debulking surgery (PDS) followed by platinum-based adjuvant chemotherapy is still the standard treatment (20). However, NACT plus interval debulking surgery (IDS) is indicated for patients with extensive tumor burden or poor surgical performance, but there is a lack of consensus regarding the best candidates for NACT (21–23).

NHB patients with ovarian cancer are more likely to present with advanced-stage disease (24) and underlying comorbidities (24) at the time of their diagnosis, and they may be more likely to receive NACT. However, the few studies that have investigated disparities in the use of NACT in NHB compared with NHW patients with ovarian cancer offered mixed results (24–30). Four of seven studies did not find any difference in the use of NACT between these two groups (24–26, 29). Only one previous study investigated the impact of NACT on racial disparities in survival and found that NHB women were more likely to receive NACT, which led the authors to hypothesize that the survival disparity for NHB may be explained by higher NACT use (30). However, the study had inadequate statistical power to evaluate this hypothesis given the small number of NHB patients included (n = 85), was based on a single institution, and included patients with stage I–IV ovarian cancer. In addition, evidence for disparities in the use of NACT among Hispanic and Asian women is scant (5). Overall, there is insufficient knowledge of racial and ethnic differences in NACT plus IDS versus PDS plus adjuvant chemotherapy use and how NACT use contributes to racial and ethnic disparities in ovarian cancer survival. Therefore, using the National Cancer Database (NCDB; ref. 31), we examined whether the use of NACT plus IDS versus PDS plus adjuvant chemotherapy varied by racial and ethnic groups among patients with ovarian cancer and whether differences in treatment sequence contributed to racial and ethnic disparities in OS.

Data source

The data for this study were extracted from the NCDB (31), a nationwide oncology outcomes database for more than 1,500 Commission on Cancer-accredited cancer programs in the United States and Puerto Rico. The NCDB is a multicenter hospital-based cancer registry containing approximately 34 million records collected from hospital cancer registries across the United States, capturing 70% or more of newly diagnosed malignancies in the United States. This study was determined to be exempt from Institutional Review Board review.

Study population

Women ages 18 and older, diagnosed with invasive stage III or IV ovarian cancer between 2004 and 2017, were included in this study. Patients with a primary diagnosis of ovarian cancer, but had one or more cancer diagnoses, were also included. We excluded patients with no surgery (n = 38,069), missing surgery (n = 456), missing chemotherapy (n = 5,937), patients with stage 0–II or unknown stage (n = 104,839), and patients who were missing information on race or ethnicity (n = 2,483; Fig. 1).

NACT was defined as the initiation of chemotherapy >21 days but ≤180 days before IDS. Adjuvant chemotherapy was defined as the initiation of chemotherapy between 1 and 120 days after PDS. Patients who started chemotherapy ≤21 days or >180 days before surgery (n = 1,809) and patients who started chemotherapy >120 days after surgery (n = 366) were excluded. Using race and ethnicity variables, we classified patients with ovarian cancer into the following mutually exclusive groups: NHW, NHB, Asian, and Hispanic women. Other racial and ethnic groups were excluded (n = 2,177).

Outcome and covariates

The primary outcome of interest was all-cause mortality (or OS). We also evaluated predictors of receiving NACT plus IDS compared with PDS plus adjuvant chemotherapy. Covariates of interest included age at diagnosis (years), insurance status (yes or no), race and ethnicity, Charlson–Deyo comorbidity index (0, 1, ≥2), treatment facility type (academic/research or nonacademic), location of treatment facility (Northeast, South, Midwest, and West), the distance of the facility from a patient's residential address at diagnosis, treatment sequence (NACT plus IDS or PDS plus adjuvant chemotherapy), histotype (high-grade serous or others), year of diagnosis (2004–2011 or 2012–2017) which was based on the sharp increase in the use of NACT after the findings from the clinical trials of NACT in late 2010, stage of cancer (stage III or IV), surgical margins (no residual tumor, residual tumor, and not evaluated/unknown), neighborhood education level, and median household income. Neighborhood education level in the NCDB is documented from matching the patient zip code recorded at the time of diagnosis with the American Community Survey 2016 (spanning years 2012–2016) and categorized into quartiles of adult ≥25 years who did not graduate from high school (≥17.6%, 10.9%–17.5%, 6.3%–10.8%, and <6.3%), which we combined into two groups (<10.9% as high education level and ≥10.9% as the low education level). Median household income in the NCDB is derived from matching the patient zip code recorded at the time of diagnosis with the American Community Survey 2016 (spanning years 2012–2016) and categorized into quartiles (<$40,227, $40,227–$50,353, $50,354–$63,332, and ≥$63,333), which we combined into two groups (≥$50,353 or <$50,353).

Statistical analysis

Descriptive characteristics by race and ethnicity were calculated as mean and SD for continuous variables and frequency and percent for categorical variables. We computed the proportion of patients receiving NACT plus IDS over time for the full cohort and by racial and ethnic groups. ORs and 95% confidence intervals (CI) were estimated using univariable and multivariable logistic regression models to identify factors associated with receiving NACT plus IDS versus PDS plus adjuvant chemotherapy.

Cox proportional hazards regression models were used to estimate HRs and 95% CI for the racial and ethnic disparities in all-cause mortality in women diagnosed with ovarian cancer. Patients in the PDS plus adjuvant chemotherapy group must survive until they receive adjuvant chemotherapy, while some of the patients in the NACT plus IDS group may die right after surgery, which could lead to overestimation of HR in favor of the PDS plus adjuvant chemotherapy group due to immortal person-time (32). For this reason, landmark analyses were employed with follow-up beginning 120 days after surgery to reduce immortal time bias and patients who died within 120 days after surgery were excluded. Survival time was measured in months beginning 120 days after the surgery to the date of death. Patients alive at last follow-up or lost to follow-up were censored. The vital status information in the NCDB is derived from the National Death Index, which contains information about death records provided by the state vital statistics office. We verified the proportional hazards assumptions by visually inspecting the log-log plots for each independent variable. No violation of the assumptions was observed. We also used the Kaplan–Meier survival curves to estimate the median survival time and compute the log-rank test to compare survival time across racial and ethnic groups. All statistical analyses were performed with SAS version 9.4 (SAS Institute).

Among the 37,566 patients with ovarian cancer included in the study, 31,023 (83%) were NHW, 3,025 (8.0%) were NHB, 1,272 (3.4%) were Asian, and 2,246 (6.0%) were Hispanic (Table 1). Receipt of NACT plus IDS was comparable across racial and ethnic groups, with 35% of NHW, 36% of NHB, 34% of Asian, and 35% of Hispanic patients receiving NACT plus IDS. Stage IV diagnoses were more common among NHB (36%), Asian (36%), and Hispanic (37%) women compared with NHW (33%) women. NHB patients were more likely to have a comorbidity score of ≥1 (poor health) compared with other racial and ethnic groups. NHB and Hispanic patients were more likely to reside in lower-income neighborhoods compared with NHW and Asian women (64% and 50% vs. 34% and 21%, respectively). The proportion of patients who received NACT plus IDS increased over time for all racial and ethnic groups (Fig. 2). Approximately 20% of patients received NACT plus IDS in 2004, which increased to 55% in 2017.

In Table 2, we present the associations of patient demographic and clinical factors with receipt of NACT plus IDS. In the multivariable-adjusted logistic regression analysis, NHB women had higher odds of receiving NACT plus IDS versus PDS plus adjuvant chemotherapy than NHW women (OR: 1.12; 95% CI: 1.02–1.22). Asian and Hispanic women also had an increased odds of receiving NACT plus IDS compared with NHW women (OR = 1.12; 95% CI: 0.99–1.28 and OR = 1.09; 95% CI: 0.98–1.20, respectively). Patients with ovarian cancer presenting with ≥2 comorbidities at diagnosis were also more likely to receive NACT plus IDS compared with those without a comorbidity (OR = 1.17; 95% CI: 1.04–1.31). Patients being treated at a community treatment facility were less likely to receive NACT plus IDS compared with those treated at an academic center (OR = 0.90; 95% CI: 0.85–0.94).

Mean follow-up time for the full cohort was 55.5 months (SD: 36.5 months), while the median survival time was 40.4 months. The median survival time was longer for Asian (53.5 months), Hispanic (51.2 months), and NHW women (39.8 months) than NHB women (35.8 months; Fig. 3).

In the univariate analysis, NHB women had higher hazard of death (HR: 1.09; 95% CI: 1.04–1.14), while Asian and Hispanic women had lower hazard of death (HR: 0.74; 95% CI: 0.68–0.80; and HR: 0.78; 95% CI: 0.73–0.83, respectively) than NHW women. In the multivariable analysis, the observed mortality disparities persisted (Table 3). NHB women had higher hazard of death compared with NHW women (HR: 1.14; 95% CI: 1.09–1.20), while Asian and Hispanic women had lower hazard of death compared with NHW women (HR: 0.81; 95% CI: 0.74–0.88; and HR: 0.83; 95% CI: 0.77–0.88, respectively). After further adjusting for treatment sequence (NACT plus IDS or PDS plus adjuvant chemotherapy), the estimates of association for all-cause mortality for NHB compared with NHW women did not change (HR: 1.14; 95% CI: 1.08–1.20). The elevated increased mortality for NHB women was similar for stage III and IV among those receiving NACT plus IDS and those receiving PDS plus adjuvant chemotherapy (Supplementary Table S1). There was essentially no difference in the HRs when cut-off points of 30, 60, and 90 days after surgery were used as the start of time for follow-up in landmark analysis (Supplementary Table S2).

In this study, we investigated the factors associated with receipt of NACT plus IDS, and the contribution of NACT plus IDS to racial and ethnic disparities in all-cause mortality in women diagnosed with ovarian cancer. We report that NHB, Asian, and Hispanic women were more likely to receive NACT plus IDS than NHW women. However, only NHB women experienced elevated hazard of all-cause mortality compared with NHW women, regardless of NACT use. Asian and Hispanic women had a lower hazard of all-cause mortality compared with NHW women.

Our results add to the existing evidence that NHB women are more likely to receive NACT plus IDS (27, 28) compared with NHW women. NACT has been used more frequently in patients with higher disease burden, comorbidities, and advanced-stage disease, all of which are more common among NHB women (30, 33). However, we did not find that treatment with NACT plus IDS relative to PDS plus adjuvant chemotherapy was a major contributing factor to the survival disparities of NHB women compared with NHW women diagnosed with ovarian cancer. Similarly, in our examination of receipt of NACT plus IDS over time, we show that uptake of NACT plus IDS was comparable across racial and ethnic groups.

Our findings that the hazard of mortality for NHB women was higher than for NHW women after adjusting for treatment (NACT plus IDS vs. PDS plus adjuvant chemotherapy) differs with what was reported in the only previous study of survival in patients with ovarian cancer after adjusting for NACT (30). The prior study found that the observed racial disparity was mitigated after adjusting for treatment. It is unclear what may account for the inconsistent results; however, one explanation is that the investigators included stage I–IV patients and analyses were not adjusted for stage at diagnosis. NACT is indicated for use in ovarian cancer with stage III/IV disease when the patient presents with ovarian cancer at an advanced age or with underlying comorbidities that would inhibit a successful surgical outcome. The previous study was a single institution-based study and had a small sample size of NHB (n = 85 among whom only 29 received NACT), which likely contributed to imprecise estimates of association.

Other studies of patients with ovarian cancer have reported higher mortality for NHB women compared with NHW women after adjusting for age, stage, comorbidity, income, and insurance (5, 34–37). Some have reported higher mortality for NHB women compared with NHW women despite receiving equivalent treatment regimens (7, 35, 38, 39). Our findings are consistent with these studies, although none of these studies adjusted for NACT plus IDS. Our results suggest that NACT plus IDS is not a major contributing factor to the increased mortality experienced by NHB women, as further adjustment for NACT plus IDS did not influence the estimates of association. Still, it is possible that NHB women in our study were more likely to have chemotherapy resistance, dose reduction, or discontinuation of chemotherapy, all of which could contribute to the higher observed mortality rates. Our findings of lower mortality for Hispanic women are consistent with the findings of a study by Ibeanu and colleagues, which reported longer survival for Hispanic women compared with NHW women (median OS: 45 vs. 36 months; ref. 14). These findings are different than what were reported in other studies, which reported no difference in OS between Hispanic and NHW women (15, 16, 30). The reason could be that these studies included patients with stage I–IV disease and one focused on patients ages ≥65 years (16). However, only one of these studies (30) adjusted for NACT, which only included 16 Hispanic women who received NACT. Our findings of lower all-cause mortality for Asian women are consistent with other studies (13, 15). One study reported a lower mortality (HR: 0.95; 95% CI: 0.91–0.99; ref. 15) and another reported improved 5-year ovarian cancer-specific survival (59% vs. 43%) based on Kaplan–Meier (13) for Asian versus NHW women. Our results did not change when we added targeted therapy to the model (HR: 1.15; 95% CI: 1.09–1.21). However, only a small proportion of the patients received targeted therapy. The treatment landscape of ovarian cancer is evolving, and more targeted treatment protocols in the use of surgery, chemotherapy, and targeted therapy are being incorporated into guidelines (40). This evolution of ovarian cancer treatment will continue as we discover predictive biomarkers and as immune therapeutics are introduced into the treatment of ovarian cancer (40). Future studies will need to incorporate these new treatment guidelines for ovarian cancer disease management into consideration.

A strength of the current study is the large and diverse study sample size, which to our knowledge is the largest study of racial and ethnic disparities in ovarian cancer mortality adjusting for the use of NACT plus IDS. Still, there are important limitations. The study lacked detailed treatment information, including regimen, dosing received, discontinuation, and residual disease, which may also be important to fully understand the contribution of treatment to racial and ethnic disparities in ovarian cancer mortality. Moreover, we did not have information regarding disease progression and underlying cause of death; therefore, we could not evaluate the associations with progression-free survival and cause-specific survival which may be important clinical endpoints for future studies. However, previous studies have shown that estimates of association using all-cause and cause-specific mortality are comparable due to the low probability of survival among patients with ovarian cancer (41). We also excluded individuals who did not receive surgery, as our primary interest was a comparison of the two treatment sequences. Patients with ovarian cancer who receive neoadjuvant chemotherapy and progress while on therapy would likely die from their disease before being eligible to receive surgery, and therefore excluded from this study. This could mean that the patients who received NACT plus IDS in our study population had less severe disease compared with the broader patient population that received NACT originally. The NCDB patient population may differ from the broader population of patients with ovarian cancer, which could lead to selection bias. However, the NCDB is a rich research resource covering approximately 70% of the population. We were also limited in the ability to look at other racial and ethnic groups, or disaggregate the racial and ethnic groupings, due to the smaller sample sizes. Nevertheless, this study is the most extensive study investigating differences in NACT use by race and ethnicity, and its contribution to known racial and ethnic disparities in all-cause mortality.

In conclusion, among women diagnosed with stage III and IV ovarian cancer, NHB, Asian, and Hispanic women were more likely to receive NACT plus IDS than NHW women. However, this difference in treatment received does not seem to explain the persistent excess mortality experienced by NHB women after an ovarian cancer diagnosis. Our results warrant further evaluation of racial and ethnic differences in NACT and possible impact on survival in a cohort of patients with more detailed treatment information.

S.A. Amin reports grants from New Jersey Commission on Cancer Research during the conduct of the study. L.J. Collin reports grants from NIH during the conduct of the study; grants from NIH outside the submitted work. S. Setoguchi reports receiving research funding from NIH, Cystic Fibrosis Foundation, PCORI, Pfizer, Inc., Pfizer Japan, BMS, and Daiichi Sankyo and serving as a consultant for Pfizer Japan, Merck Co., Inc., BMS, and Medtronic, Inc. J.M. Satagopan reports grants from NIH during the conduct of the study; and J.M. Satagopan's time and effort were supported in part by NIH/NCI grant R01 CA197402. E.V. Bandera reports grants from NIH and New Jersey Commission on Cancer Research during the conduct of the study; personal fees from Pfizer, Inc. outside the submitted work. No disclosures were reported by the other author.

The funding organizations had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the article; and decision to submit the article for publication.

S.A. Amin: Conceptualization, formal analysis, supervision, funding acquisition, methodology, writing–original draft. L.J. Collin: Conceptualization, formal analysis, supervision, funding acquisition, methodology, writing–original draft. S. Setoguchi: Conceptualization, methodology, writing–original draft, writing–review and editing. J.M. Satagopan: Conceptualization, methodology, writing–original draft, writing–review and editing. A. Buckley de Meritens: Conceptualization, methodology, writing–original draft. E.V. Bandera: Conceptualization, supervision, funding acquisition, methodology, writing–original draft.

This work was funded by grants NIH R01CA243188 (E.V. Bandera) and New Jersey Commission on Cancer Research COCR22PDF007 (S.A. Amin). L.J. Collin was supported by TL1TR002540 from the National Center for Advancing Translational Sciences of the NIH.

The publication costs of this article were defrayed in part by the payment of publication fees. Therefore, and solely to indicate this fact, this article is hereby marked “advertisement” in accordance with 18 USC section 1734.

Note: Supplementary data for this article are available at Cancer Epidemiology, Biomarkers & Prevention Online (http://cebp.aacrjournals.org/).

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