Association of Care at Minority-Serving vs Non–Minority-Serving Hospitals With Use of Palliative Care Among Racial/Ethnic Minorities With Metastatic Cancer in the United States

IMPORTANCE It is not known whether racial/ethnic differences in receipt of palliative care are attributable to different treatment of minorities or lower utilization of palliative care at the relatively small number of hospitals that treat a large portion of minority patients. OBJECTIVE To assess the association of receipt of palliative care among patients with metastatic cancer with receipt of treatment at minority-serving hospitals (MSHs) vs non-MSHs. DESIGN, SETTING, AND PARTICIPANTS This retrospective cohort study used Participant Use Files of the National Cancer Database, a prospectively maintained, hospital-based cancer registry consisting of all patients treated at more than 1500 US hospitals, to collect data from individuals older than 40 years with metastatic prostate, lung, colon, and breast cancer, diagnosed from January 1,2004,toDecember31,2015.DatawereaccessedinOctober2017,andtheanalysiswasperformed in July 2018. EXPOSURES Hospitals in the top decile in terms of the proportion of black and Hispanic patients for each cancer type were defined as MSHs. MAIN OUTCOMES AND MEASURES A multilevel logistic regression model that estimated the odds of palliative care was fit, adjusting for year of diagnosis, sex, race/ethnicity, insurance, income, educational level, and cancer type, with an interaction term between cancer type and MSH status and a hospital-level random intercept to account for unmeasured hospital characteristics. RESULTS A total of 601680 individuals (mean [SD] age, 67.4 [11.4] years; 95% CI, 67.2-67.6 years; 314279 [52.2%] male; 475039 [78.9%] white)


Introduction
Palliative care plays a central role in the management of advanced cancer.Despite advances in targeted chemotherapy and immunotherapy, cancer remains the second leading cause of death in the United States, 1 and most patients with metastatic cancer will ultimately die of their disease.For these patients, receipt of palliative care is associated with improved quality of life and prolonged survival. 2e presence of race/ethnicity-based disparities in health care and health outcomes is well documented.Racial/ethnic minorities often receive worse care and have worse outcomes. 3In cancer specifically, there are disparities in screening, 4 treatment, 5,6 and survival. 7Race/ethnicity-based differences have also been found in receipt of end-of-life care. 8,94][15][16][17] Because hospital care for most minority patients is concentrated at a comparatively small number of facilities, 18 differences in care at these minority-serving hospitals (MSHs) could explain worse population-level outcomes for minorities overall.If so, policies to improve care at these hospitals represent a potential strategy to address race/ethnicity-based disparities.
We assessed racial/ethnic differences in receipt of palliative care for individuals diagnosed with metastatic prostate, lung, colon, and breast cancer.We examined whether receipt of palliative care differed by site of care and whether racial/ethnic disparities in receipt of palliative care are associated with minority patients receiving treatment in a subset of hospitals where palliative care is less often provided.

Data Source
The data for this study were abstracted from the Participant Use Files of the National Cancer Database (NCDB), a US cancer registry combining data on patients seen at any 1 of 1500 Commission on Cancer-accredited institutions in the United States. 19The NCDB registry is a joint project of the American Cancer Society and the Commission on Cancer of the American College of Surgeons, comprising more than 29 million unique cases.Trained data abstractors use standardized methods to collect sociodemographic and clinical data, including tumor type, stage, grade, and treatments. 20e NCDB captures 50.8% of all prostate cancers, 82.1% of all lung cancers, 62.5% of all colon cancers, and 66.6% of all breast cancers diagnosed in the United States. 21Data were accessed in October 2017, and the analysis was performed in July 2018.The study was approved by the Brigham and Women's Hospital Institutional Review Board under a general study protocol for analyses using NCDB data, which included a waiver of informed consent because the information in the Commission on Cancer's NCDB is deidentified.This study conformed to the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guideline for reporting observational research. 22

Study Cohort
We chose to focus on men and women 40 years and older with metastatic prostate, non-small cell lung, colon, and breast cancer.These 4 cancer types were chosen because they represented the most common and most lethal cancers for men and women during the study period. 23We chose prostate C619, lung C340 to C349, colon C180 to C189 and C260, and breast C500 to C509.We selected men and women with confirmed distant metastases based on the American Joint Committee on Cancer staging system. 24We excluded individuals who had missing follow-up information as well as those diagnosed when younger than 40 years because facility information on these patients is censored by the NCDB for confidentiality purposes.

Receipt of Palliative Care
The main outcome measure was receipt of any palliative care services.Receipt of palliative care is a variable included with the Participant Use Files of the NCDB.Receipt of palliative care is determined by NCDB data abstractors based on patients' clinical medical records at participating institutions.
Treatments are coded as palliative only if it is explicitly mentioned that the goal of treatment is palliation and not cure (eg, pain control after a routine surgical procedure would not be coded as palliative care).Palliative care encompasses surgical treatment, radiation therapy, and systemic chemotherapy administered to alleviate symptoms but not to cure. 25 For the purposes of this study, palliative care was treated as a dichotomous variable.

MSH Status
The site of care was the facility reporting the case to the NCDB.This facility is typically the site of diagnosis.For those who received care at multiple institutions, the site of care was the facility where they received definitive cancer care.The MSH status was calculated for each facility based on the proportion of minority patients as follows.First, hospitals were ranked in terms of the proportion of minority patients (black or Hispanic).Second, we identified hospitals in the top decile when ranked from least to greatest proportion of minority patients. 26,27Hospitals in the top decile were considered MSHs.We used the entire population with a diagnosis, not limiting to metastatic cancer only (eg, number of black and Hispanic men with prostate cancer [any stage] at an institution as a portion of the total number of men with prostate cancer [any stage] at that institution and so forth).

Covariates
Baseline  30 We used χ 2 tests with a Rao-Scott adjustment to account for clustering to compare the distribution of covariates between patients treated at MSHs and non-MSHs. 31,32We then performed a univariate analysis, again clustering by facility, to compare the proportion of patients receiving palliative care based on race/ethnicity and other baseline characteristics (eg, site of care, cancer type).
To assess the association among site of care, patient characteristics, cancer type, and palliative care, a multilevel logistic regression model was fit using the entire study population.This model included fixed-effect terms for patient clinical and demographic covariates (including race/ethnicity and cancer type) and site of care (MSH vs non-MSH).We included an interaction term between cancer type and MSH status to assess whether the effect of MSHs differed in a statistically significant fashion among the 4 cancer types.A facility-level random intercept was included to account for unmeasured hospital-level characteristics that might cut across multiple cancers. 33For example, some hospitals may have palliative care departments, whereas others may not.
Finally, based on a significant interaction term (between MSH and cancer type), we performed subgroup analyses by cancer type.For each cancer type, we fit separate multilevel models that assessed the association of clinical and demographic variables as well as site of care on the odds of receiving palliative care.
All analyses were performed with Stata statistical software, version 14.0 (StataCorp).Statistical significance was defined as a 2-sided P < .05.

Results
The study cohort consisted of 601 680 individuals (mean [SD] age, 67.4 [11.4]The interaction term between cancer type and MSH status was associated with receipt of palliative care.Thus, we performed a subgroup analysis stratifying by cancer type.In the metastatic prostate cancer subgroup, the odds of receiving palliative care at MSHs were approximately 33% lower (OR, 0.67; 95% CI, 0.55-0.82); in the lung cancer subgroup, the odds of palliative care were 27% lower at MSHs (OR, 0.73; 95% CI, 0.57-0.93); in colon cancer, the odds of palliative care at MSHs were not significantly lower (OR, 0.86; 95% CI, 0.67-1.09);and in breast cancer, the odds of palliative care were 27% lower (OR, 0.73; 95% CI, 0.59-0.89).As in the combined cohort, adjustment for MSH status in all cancers attenuated the association between race/ethnicity and odds of receiving palliative care toward the null.

Discussion
In this retrospective, registry-based study of adults diagnosed with metastatic prostate, lung, breast, and colon cancer, there were significantly lower odds of receiving palliative care among patients treated at MSHs compared with non-MSHs.Although it has been previously reported that minority patients are less likely to receive palliative care services at the end of life, 8,9 the present findings suggest that site of care may be a significant factor associated with race/ethnicity-based differences in palliative care.
The policy implications of this finding are significant.Given that care for minority patients is concentrated at a comparatively small number of hospitals in the United States, it is likely that one important strategy to address racial/ethnic disparities in palliative care is to focus on improving access to palliative care at the small number of hospitals that care for most minority patients.If initiatives to target palliative care use at MSHs are successful, national disparities in palliative care may be reduced.
Overall, this fits with an increasing understanding that the site of care is a determinant of health outcomes for minority patients.Although there are data that physicians may systematically treat black and white patients differently, 11,12 that minority patients tend to receive care at different facilities is also important.More than being a function of individual behavior, there is increasing recognition that disparities in outcomes depend on different treatment of white and minority patients within the same hospital and systemic differences in where minority patients receive care. 14,15previous study 18 found that MSHs have higher readmission rates and worse performance in many clinical scenarios, for example, when treating acute myocardial infarctions and pneumonia.A  35 An analysis 36 of racial disparity in surgical mortality found that although gaps between black and white patients have narrowed overall, improvements were less likely among hospitals that served the highest proportion of minority patients.Overall, our findings suggest that similar differences between MSHs and non-MSHs may be associated with the differences in receipt of palliative care among underserved minority patients.
Although Asian patients composed a small proportion of our population, they were less likely to receive palliative care after adjusting for MSH status.Asian individuals are a heterogeneous group and may in some cases have better access to health care compared with Hispanic patients and black patients; Asian individuals have population-level health outcomes that exceed most of the other racial/ethnic groups. 37Thus, as has been done in a prior study, 27 we did not include Asian patients in our definition of MSHs.The lower odds of palliative care among Asian patients could reflect cultural differences, differences in familial characteristics among this population, and other economic or health systems factors.
The finding that palliative care is more common in Medicaid patients and uninsured patients was similarly surprising given that these patients seem to receive worse care based on many other health metrics. 38Perhaps these patients were presenting at a more advanced stage of disease, when palliative care is the only good option.Alternatively, perhaps the absence of a strong fee-for-service incentive toward doing more reduced the barrier for palliative care for the Medicaid and uninsured patients.

Strengths and Limitations
Strengths of our study include our use of a large, accurate national registry, which captures most US patients diagnosed with 4 highly prevalent types of cancers.Another strength is that our study included patients from all payers.Our work therefore improves on earlier definitions of minority serving, which often used Medicare claims and therefore involved only the proportion of Medicare beneficiaries who were racial/ethnic minorities not the proportion of patients with a given condition. 26spite these strengths, this work has limitations.Data on palliative care services are of uncertain accuracy.The data on receipt of palliative care in the NCDB were collected from medical records by trained data abstractors at each institution.Intent must be inferred from clinical records.
Although we believe that record review may be more accurate than insurance claims, which have been reported to often have only moderate accuracy for ascertaining the intensity of end-of-life care, 39 the accuracy may be lower than some prospective trials that have specifically assigned (eg, some hospitals may have palliative care departments, whereas others may not).
Although the NCDB captures most patients with each of these 4 cancer types in the United States, data are not population based.Thus, certain patients who did not receive care at Commission on Cancer-accredited US hospitals may have been underrepresented.For example, if the database underrepresents poor-performing, rural non-MSHs, the disparities among MSHs could be inflated.

Conclusions
These findings suggest that there are significant racial/ethnic disparities in receipt of palliative care for metastatic cancer within a large cohort of US patients with cancer.After controlling for race/ ethnicity and MSH status, we found that treatment at MSHs was associated with significantly lower odds of receiving palliative care, but black and Hispanic race/ethnicity was not.Strategies that focus on improving palliative care use at MSHs may be an effective strategy to increase the receipt of palliative care for this population.

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, and a maximum likelihood technique for our multilevel model was used to address this.

Table 2 .
Unadjusted Proportions of Patients With Metastatic Cancer Receiving Palliative Care in Overall Cohort by Baseline Characteristics (continued) Site of Care and Use of Palliative Care Among Racial/Ethnic Minorities With Metastatic Cancer Downloaded From: https://jamanetwork.com/ on 09/28/2023

Table 3 .
Factors Associated With Palliative Care in an Adjusted Multilevel Model Including a Hospital-Level Random Intercept Site of Care and Use of Palliative Care Among Racial/Ethnic Minorities With Metastatic Cancer Downloaded From: https://jamanetwork.com/

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34of emergency general surgery at MSHs found that hospital-level factors accounted for approximately 40% of increased odds for readmission, and inpatient mortality was significantly greater.Hospital leadership can also play an important role.A survey of chairmen at black-serving hospitals found that, when compared with non-black-serving hospital boards, these chairpersons report less expertise with quality-of-care issues and are less likely to give high priority to quality of care.

Table 3 .
2actors Associated With Palliative Care in an Adjusted Multilevel Model Including a Hospital-Level Random Intercept (continued)Site of Care and Use of Palliative Care Among Racial/Ethnic Minorities With Metastatic Cancer patients to palliative care interventions.2Additionalstudies that specifically address interrater variability and validate this variable against other end points (eg, inappropriately aggressive end-oflife care, such as chemotherapy in the last 14 days of life, death in hospital, or death in the intensive care unit) would be useful.Another limitation is the possibility of unmeasured patient confounders, which are always a factor in retrospective research.Our use of a multilevel model with a hospital-level random intercept should account for unmeasured hospital characteristics at the level of the hospital a Estimated from county of residence.JAMA Network Open | OncologyJAMA Network Open.2019;2(2):e187633.doi:10.1001/jamanetworkopen.2018.7633(Reprinted) February 1, 2019 10/13 Downloaded From: https://jamanetwork.com/ on 09/28/2023