Background
Ovarian cancer (OC) is the fifth leading cause of cancer-related death and the deadliest gynecologic cancer in the United States, with an estimated 5-year survival rate of 49.1%.1,2 White women experience the highest incidence of OC (11.3/100,000), followed by Hispanic (10.3/100,000) and Black (9.0/100,000) women.2 Although survival rates improved for White women from 1973 to 2007 (36%–44%), they worsened for Black women (42%–36%),2,3 partly due to lack of receipt of guideline-concordant treatment.
Racial disparities in receipt of guideline-concordant care have been well described. Black women are less likely to receive care that is concordant with the NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines) for OC, including cancer-directed surgery and chemotherapy.3–8 National guidelines for the treatment of advanced-stage OC recommend surgical staging and cytoreduction plus systemic chemotherapy.9 Maximal cytoreductive surgery correlates with improved survival outcomes, and lack of concordance with the NCCN Guidelines is an independent predictor of worse survival.6,10,11 Some evidence suggests that equal care leads to similar outcomes among Black and White women with advanced OC12,13; however, other large analyses have reported that although receipt of guideline-concordant treatment was associated with substantially improved outcomes in both Black and White women, some racial disparities in OC survival persist.6,10,11
Given the well-documented survival advantage associated with receipt of guideline-concordant treatment and the reduced rates of guideline-concordant treatment receipt among Black patients, elucidating the healthcare access (HCA) factors driving racial inequities in receipt of guideline-concordant care is imperative to help narrow the survival disparity in OC. The Penchansky and Thomas framework describes 5 dimensions of HCA: affordability (ability to pay), availability (type, quality, and volume of services), accessibility (geographic location of services), accommodation (organization of services, patient resources), and acceptability (patient experience, quality of patient–provider interaction).14 Although prior studies have examined the association of individual components of HCA dimensions (eg, socioeconomic status [SES], facility volume, and insurance status) with guideline-concordant care,15–18 none have comprehensively evaluated multiple dimensions simultaneously among a diverse group of patients with OC. This study evaluated the association of 3 HCA dimensions measurable in the SEER-Medicare linked database (affordability, availability, and accessibility) in relation to racial/ethnic disparities in receipt of guideline-concordant treatment of OC.
Methods
Overview
We conducted an observational cohort study of the association between HCA dimensions and receipt of recommended OC treatment based on clinical guidelines relevant for each patient’s tumor characteristics. The main outcomes assessed were receipt of surgery among patients for whom surgery was recommended and receipt of systemic therapy if recommended.
Study Population
Non-Hispanic (NH)–Black, Hispanic, and NH-White women aged ≥65 years diagnosed with primary OC (SEER primary site code C569) in 2008 through 2015 were selected from the SEER-Medicare linked dataset (Figure 1). Patients were required to have at least 12 months of continuous enrollment in Medicare fee-for-service Parts A and B before diagnosis; at least one Medicare inpatient, outpatient, or carrier claim with a diagnosis code for OC (ICD-9-CM 183.0 and ICD-10-CM C569) within 2 months of SEER diagnosis; and continuous fee-for-service Medicare enrollment in the 12 months after diagnosis date or until death. Patients with fallopian tube cancer, borderline tumors, or peritoneal cancers were excluded. Those who died of OC in the first year after diagnosis were excluded to allow for evaluation of receipt of treatment; patients who died of a cause other than cancer were included. Patients were excluded if they were missing any variables used to calculate HCA dimension scores or determine guideline-concordant treatment. For analyses of receipt of guideline-concordant systemic therapy, the cohort was limited to patients with a diagnosis for which the NCCN Guidelines recommended the treatment. Decision trees for exclusions based on treatment guidelines are outlined in Figures 2 and 3.
Participant flow chart for NH-Black, Hispanic, and NH-White patients with OC per SEER-Medicare 2008 to 2015. The proportion of NH-Black patients is presented for sensitivity purposes.
Abbreviations: FFS, fee-for-service; HCA, healthcare access; NH, non-Hispanic; OC, ovarian cancer.
aUsed to set the actual diagnosis date because SEER only has month/year of diagnosis.
Citation: Journal of the National Comprehensive Cancer Network 20, 11; 10.6004/jnccn.2022.7055
Decision tree for guideline-concordant primary treatment of epithelial ovarian cancer.
Simplified and adapted from the NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines) for Ovarian Cancer, Version 2.2013. This diagram does not reflect the full NCCN recommendations and is limited to clinical information and treatments that can be assessed in the SEER-Medicare database. Abbreviations: HIPEC, hyperthermic intraperitoneal chemotherapy; TAH, total abdominal hysterectomy.
aNCCN Guidelines specifically recommend 3–6 cycles of intravenous platinum doublet.
bNCCN Guidelines specifically recommend 6–8 cycles of intravenous platinum doublet.
Adapted from Morgan RJ, Alvarez RD, Armstrong DK, et al. NCCN Clinical Practice Guidelines in Oncology: Ovarian Cancer, Version 2.2013; with permission. For the most recent version of these guidelines, visit NCCN.org.
Citation: Journal of the National Comprehensive Cancer Network 20, 11; 10.6004/jnccn.2022.7055
Decision tree for guideline-concordant primary treatment of less common histologic types.
Simplified and adapted from the NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines) for Ovarian Cancer, Version 2.2013. This diagram does not reflect the full NCCN treatment recommendations and is limited to initial treatment recommendations and clinical information and treatments that can be assessed in the SEER-Medicare database.
Abbreviation: BEP, bleomycin/etoposide/platinum.
aNCCN Guidelines specify initial observation for stage I dysgerminoma, but also specify that 3 cycles of etoposide/carboplatin are appropriate for select patients with stage IB–III dysgerminoma. In this study, we did not require patients with stage IB/IC dysgerminoma to receive guideline-concordant chemotherapy because we could not identify the patient population for which it was appropriate in the SEER-Medicare database.
bNCCN Guidelines specifically recommend 6–8 cycles of intravenous platinum doublet.
Adapted from Morgan RJ, Alvarez RD, Armstrong DK, et al. NCCN Clinical Practice Guidelines in Oncology: Ovarian Cancer, Version 2.2013; with permission. For the most recent version of these guidelines, visit NCCN.org.
Citation: Journal of the National Comprehensive Cancer Network 20, 11; 10.6004/jnccn.2022.7055
SEER Patient Demographics and Clinical Characteristics
Patient and clinical characteristics from SEER data included race, ethnicity, age at diagnosis, stage at diagnosis, histology at diagnosis, marital status, geographic region of residence, and residence in a metropolitan area. We used validated coding algorithms to assess patient comorbidities and calculate the Charlson-Deyo comorbidity index score in the 12 months before OC diagnosis (supplemental eAppendix 1, available with this article at JNCCN.org).19,20
HCA Dimension Scores
A total of 35 patient, census tract, and regional-level variables (supplemental eAppendix 2) measuring dimensions of healthcare affordability (ie, census tract poverty rates, educational attainment), availability (ie, number of hospitals/specialists available per capita), and accessibility (ie, residence in metropolitan/rural area, distance traveled to care) were assessed, and confirmatory factor analysis (CFA) was used to identify the most influential variables for each aspect of HCA and create composite scores of affordability, availability, and accessibility. These findings have recently been corroborated by our group (unpublished data, 2022). Factor loadings from CFA were used to generate HCA domain scores ranging from −3 to 4. Lower values represented lower access for the dimension (ie, lower availability scores corresponded with fewer physicians and hospitals in the patient’s region of residence). CFA for HCA domains is described in supplemental eAppendix 3.
Receipt of Guideline-Concordant Surgery
Patients were considered to have received any OC-directed surgery if they had a Medicare claim that indicated an ovarian surgical procedure (supplemental eAppendix 4) 2 months before or 6 months postdiagnosis or had OC primary site surgery documented in the SEER registry data. Receipt of guideline-concordant surgery was adapted from the NCCN Guidelines (Figures 2 and 3). We considered guideline-concordant surgery to involve the receipt of comprehensive staging laparotomy, including total abdominal hysterectomy (if no prior hysterectomy), bilateral salpingo-oophorectomy, lymph node dissection (if applicable), omentectomy, and pelvic or para-aortic lymph node biopsy (for stages I–IIIB). Receipt of procedures in administrative claims data were difficult to accurately assess; therefore, we selected a subset of surgical codes that we had high confidence represented receipt of guideline-concordant OC surgery and categorized these procedures as such (supplemental eAppendix 5). Because this definition likely excluded some surgeries meeting recommendations that were coded less specifically, we conducted a sensitivity analysis including a second subset of codes that might or might not represent receipt of guideline-concordant surgery (supplemental eAppendix 5).
Initiation and Completion of Guideline-Concordant Systemic Therapy
We adapted the 2013 NCCN Guidelines (Figures 2 and 3) to determine the recommended systemic therapy by tumor characteristics.21 We examined 3 outcomes: initiation of any systemic therapy, initiation of recommended regimen, and completion of recommended cycles. Patients were considered to have initiated guideline-concordant systemic therapy if they had ≥1 Medicare claim for administration of recommended systemic therapies for the patient’s stage, grade, and histology (Figures 2 and 3, supplemental eAppendix 6) within 12 months postdiagnosis.21 Patients were considered to have completed the recommended therapy cycles if they had the recommended number of therapy administration claims at least 20 days apart within 12 months postdiagnosis. Extended duration between cycles was not penalized in this analysis.
Statistical Analysis
The distribution of patient demographics, clinical characteristics, HCA scores, and treatment receipt was calculated for the full cohort and stratified by patient race; group-level differences were tested using Kruskal-Wallis and Cochran-Mantel-Haenszel tests. Univariable- and multivariable-adjusted Cox proportional hazards regression models were used to estimate cause-specific hazard ratios (HRs) for patient race and HCA scores with (1) receipt of any surgery and (2) initiation of any systemic therapy, accounting for the competing risk of death from another cause. Multivariable-adjusted modified Poisson regression with robust error estimation was used to assess relative risk (RR) associations between patient race, HCA scores, and the following treatment outcomes: (1) receiving ≥1 cycle of guideline-recommended systemic therapy, (2) completing the recommended cycles of therapy within 12 months of diagnosis, and (3) receiving guideline-concordant surgery.22 Poisson regression was used to estimate RR instead of logistic regression because of the high prevalence of the measured outcomes (>10%).22 For the sensitivity analysis, multivariable-adjusted multinomial regression was used to assess associations between HCA dimension scores and the categorical outcome of receiving guideline-concordant surgery, receiving surgery that may or may not have met guidelines, or not receiving surgery meeting guidelines. All multivariable models were adjusted for age at diagnosis, stage at diagnosis, tumor histology, US Census region of residence, number of comorbidities, year of diagnosis, and whether the patient died of causes other than OC in the 12 months postdiagnosis.
Results
Study Population and Clinical Characteristics
The cohort included 5,632 patients with OC diagnosed from 2008 to 2015; 333 (5.9%) were NH-Black, 318 (5.6%) were Hispanic, and 4,981 (88.4%) were NH-White (Table 1). We found that 84% of NH-White patients had type II epithelial histology, compared with 81% each of NH-Black and Hispanic patients. NH-Black and Hispanic patients had a higher comorbidity burden than NH-White patients (P<.001).
Baseline Patient Characteristics (N=5,632)
Racial Differences in Affordability, Availability, and Accessibility
NH-Black patients had lower affordability and availability scores than NH-White patients (P<.001) and thus were more likely to be dual-enrolled in Medicaid and Medicare, live in financially deprived areas, and live in areas with fewer/poorer-quality healthcare resources (Table 1). However, Hispanic and NH-Black patients had higher accessibility scores than NH-White patients and were thus more likely to live in urban, denser areas.
Rates of Treatment Receipt by Patient Race and/or Ethnicity
Among patients eligible for surgery (Figure 4; n=5,632), 79% received any OC surgery within 2 months before through 6 months after diagnosis, with NH-Black patients less likely to receive any surgery (72%) compared with NH-White (79%) or Hispanic patients (82%). Approximately 45% of patients received guideline-concordant surgery, with NH-Black patients receiving this at lower rates (37%; P=.005). Among patients eligible for systemic therapy based on stage, grade, and histology at diagnosis (n=5,299), 80% initiated guideline-concordant therapy within 12 months of diagnosis. NH-Black patients were less likely to initiate guideline-concordant systemic therapy (74%) compared with NH-White (81%) and Hispanic (84%) patients (P=.005). Of those eligible for chemotherapy, 44% of NH-White and Hispanic patients and 36% of NH-Black patients received all recommended cycles. Only 24% of NH-White and Hispanic patients and 14% of NH-Black patients received both guideline-concordant surgery and completed chemotherapy.
Receipt of treatment by patient race among patients who did not die of ovarian cancer in the first 12 months following their diagnosis (n=5,362 for surgical outcomes; n=5,229 for systemic therapy outcomes).
Citation: Journal of the National Comprehensive Cancer Network 20, 11; 10.6004/jnccn.2022.7055
Receipt of Guideline-Concordant Surgery
After adjusting for patient demographic and clinical characteristics and HCA dimension scores (Table 2), neither patient race and/or ethnicity nor HCA scores were independently associated with any surgery receipt. In fully adjusted regression models assessing the receipt of guideline-concordant surgery, patients with higher affordability (RR, 1.05; 95% CI, 1.01–1.08) and availability (RR, 1.06; 95% CI, 1.02–1.10) were more likely to receive guideline-concordant surgery (Table 3). In sensitivity analyses comparing patients who received no surgery or guideline-nonconcordant surgery versus those who received guideline-concordant surgery or surgery that may or may not have met guidelines, patients with higher affordability (RR, 1.16; 95% CI, 1.06–1.26) and availability scores (RR, 1.13; 95% CI, 1.02–1.25) were more likely to receive guideline-concordant surgery (supplemental eTable 1).
Hazard Ratio for Receiving Any OC Surgery and Systemic Therapy
Relative Risk for Receipt of Guideline-Concordant Surgery Among Patients Surviving Their Ovarian Cancer at Least 12 Months (N=5,632)
Receipt of Guideline-Concordant Systemic Therapies
NH-Black patients were less likely to initiate systemic therapy than NH-White patients (HR, 0.86; 95% CI, 0.75–0.99) within 12 months of diagnosis after adjustment for patient demographic and clinical characteristics and HCA dimension scores (Table 2), and nearly all patients initiating systemic therapy received at least one round of guideline-concordant chemotherapy (Figure 4). Higher affordability scores were associated with initiation of any systemic therapy (HR, 1.10; 95% CI, 1.07–1.14) when accounting for competing risks of death from another cause (Table 2). Point estimates from Poisson RR models suggest that NH-Black patients were less likely to receive at least one cycle of guideline-concordant chemotherapy or to complete all cycles of chemotherapy, but confidence intervals crossed the null after adjustment for patient clinical characteristics (Table 4). HCA scores were not associated with the relative risk of initiating or completing guideline-concordant chemotherapy (Table 4).
Relative Risk for Receipt of Recommended Chemotherapy Among Patients Who Survived Their Ovarian Cancer at Least 12 Months (N=5,229)
Receipt of Both Guideline-Concordant Surgery and Systemic Therapies
In models adjusted for patient demographic and clinical characteristics and HCA scores, NH-Black patients were less likely than NH-White patients to receive both guideline-concordant surgery and chemotherapy (odds ratio, 0.59; 95% CI, 0.42–0.84; supplemental eTable 2). Higher availability was associated with greater likelihood of receiving guideline-concordant care (odds ratio, 1.15; 95% CI, 1.05–1.27).
Discussion
In this retrospective cohort study of patients aged ≥65 years with OC in the SEER-Medicare database, only 24% of NH-White and 14% of NH-Black patients received both guideline-concordant surgery and the recommended number of chemotherapy cycles. NH-Black patients had scores indicating lower HCA affordability and availability compared with NH-White patients. Patients with higher affordability and availability scores were more likely to receive guideline-concordant surgery and initiate systemic therapy. After accounting for demographic and clinical characteristics and all 3 HCA scores, we found that NH-Black patients were less likely to initiate systemic therapy than NH-White patients.
Our results are striking, given that prior studies found that 57% to 68% of White women and 39% to 54% of Black women with OC completed guideline-concordant care.23,24 These differences are likely driven by our use of a more stringent coding definition of guideline-concordant treatment than prior administrative claims–based studies, and our inclusion of patients with stage I and II disease who had recommendations for treatment based on the NCCN Guidelines. For example, we considered surgery codes as guideline-concordant if they included bilateral salpingo-oophorectomy plus omentectomy or a malignancy-specific code including oophorectomy and lymph node biopsies, whereas previous studies included a much broader range of surgical codes, including codes for wedge or partial resection of the ovary. Although our stringent coding may explain striking differences in receipt of guideline-concordant treatment compared with other studies, we suspect that low rates of receipt of guideline-concordant treatment in our study and prior studies could be driven by the influence of poor healthcare access, in addition to patient comorbidities, and the older age and frailty of patients diagnosed with advanced-stage disease in the Medicare population.25 We observed similar rates of any receipt of cancer-directed surgery and any receipt of chemotherapy as in prior studies.
Efforts to equalize access to guideline-concordant treatment are key to eliminating disparities in OC survival; there is an increased mortality risk among those who do not receive guideline-concordant treatment and among Black individuals independent of receipt of guideline-concordant treatment.6,8,15,24,26,27 Studies have demonstrated that Black populations have worse survival due to barriers to receipt of quality care,28,29 including late diagnosis, higher comorbidity burden,30 and less access to high-volume surgeons.31,32 HCA is well recognized as a fundamental contributor to receipt of appropriate OC treatment, but most prior studies only evaluated one dimension or component of HCA,31,33–35 whereas this study attempts to comprehensively capture multiple dimensions of HCA. We found that patients with higher affordability were more likely to receive guideline-concordant surgery and initiate and complete chemotherapy, which is consistent with past findings that low SES is associated with lower likelihood to undergo surgery or receive chemotherapy.28 We found that patients of minority race had lower availability scores and that higher availability of healthcare resources was associated with increased likelihood of undergoing guideline-concordant surgery; past studies have also reported that patients of minority race and low SES are more likely to receive care at low-volume hospitals with low-volume physicians, which are components of HCA availability.34 These results highlight the importance of increasing the number of affordable, high-quality healthcare facilities in minority neighborhoods. Patients who live in rural settings, a measure of lower accessibility, have poorer survival compared with their urban counterparts.36 In our study, Hispanic and NH-Black patients had higher accessibility scores compared with NH-White patients. Although distance and availability of specialists may be a larger issue for White patients who are more likely to live in rural areas, NH-Black and Hispanic patients who live in urban areas may have other challenges, including transportation to appointments.
Importantly, we observed that racial disparities in the initiation of systemic therapy persisted even after adjusting for HCA dimensions. Therefore, simply addressing differences in these dimensions may be insufficient to ameliorate racial disparities in treatment. Two HCA dimensions remain unaccounted for in our study: accommodation (coordination and convenience of care) and acceptability (quality of patient–provider interactions).14 Although they cannot be estimated in the SEER-Medicare dataset, these dimensions encompass measures of patient-centered care—communication, cultural competence, implicit bias, and discrimination—that may be an important moderator of the association between other HCA dimensions and treatment outcomes. For example, perceived discrimination is associated with decreased healthcare utilization, lower adherence to medical recommendations,37,38 and prolonged symptom duration before OC diagnosis among NH-Black women.39 Future studies that examine acceptability and accommodation are necessary to fully characterize HCA in relation to treatment.
This study highlights the role of race and HCA in receipt of appropriate OC treatment. However, administrative claims data cannot provide the full clinical picture that physicians use to make treatment recommendations and/or account for patient preferences. The SEER database is limited in the specificity available for measures of HCA; most measures are calculated at the area level and may not accurately reflect individual circumstances. The HCA scoring system and treatment guideline–concordance were not clinically validated, limiting interpretations of the data. Although we did not examine the timeliness of receipt of therapy or dose intensity, delays in chemotherapy completion can negatively impact survival.40,41 The strengths of our analysis include a racially diverse population, large sample size, and comprehensive evaluation of HCA accessibility, availability, and affordability.
Conclusions
HCA affordability and availability were associated with guideline-concordant treatment. However, NH-Black patients were less likely to initiate systemic therapy compared with NH-White patients even after accounting for HCA dimensions. Further research on other HCA dimensions and a thorough examination of facilitators and barriers to treatment are needed to enhance delivery of optimal treatment and close the racial gap in survival for patients with OC.
Acknowledgments
The authors acknowledge the helpful assistance provided by the SEER-Medicare reviewers, information management system coordinator Elaine Yanisko, and all the patients whose valuable data contributed to this study.
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