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Abstract

Background

Access to care has been implicated in racial-ethnic disparities in surgical treatment and survival for patients with renal cell carcinoma (RCC) in the United States. We assessed whether there were racial-ethnic disparities in surgery receipt and clinical outcomes of RCC in the equal access U.S. Military Health System (MHS).

Materials and Methods

We used the MilCanEpi database to study a cohort of patients aged 18 and older who were diagnosed with stage I-III RCC between 1998 and 2014. Treatment with nephrectomy was evaluated in Poisson regression models expressed as adjusted incidence rate ratios (AIRRs) with 95% confidence intervals (CIs). Risk of recurrence and all-cause death were estimated using multivariable Cox regression models.

Results

The study included 1371 non-Hispanic White, 362 non-Hispanic Black, and 177 Hispanic patients. Black patients had lower rates of nephrectomy compared to non-Hispanic White patients overall (AIRR = 0.83, 95% CI = 0.72, 0.95) and in strata for stage I (AIRR = 0.74, 95% CI = 0.64, 0.87) or clear cell subtype (AIRR = 0.57, 95% CI = 0.42, 0.77). Hispanic patients had similar overall rates of nephrectomy as non-Hispanic White patients (AIRR = 1.16, 95% CI = 0.98, 1.37) and higher rates among those with clear cell RCC (AIRR = 1.40, 95% CI = 1.01, 1.96). Black patients had lower risk of recurrence (AHR = 0.61, 95% CI = 0.41, 0.92) relative to non-Hispanic White patients with no other racial-ethnic differences in outcomes in multivariable models.

Conclusion

In the equal access MHS, there were some significant variations in rates of nephrectomy between racial-ethnic groups overall and among patient subgroups by tumor stage and histology. Despite observed lower surgery rates among non-Hispanic Black patients, the risk of recurrence or survival was lower or equal as compared to non-Hispanic White patients with non-metastatic RCC. Further research on factors other than access to care that may explain the differences in treatment and outcomes among racial-ethnic groups is needed.

Keywords

renal cell carcinoma nephrectomy racial disparity recurrence survival

Introduction

Kidney cancers are one of the top-10 most common cancers in terms of incidence for both men and women in the United States with about 85-90% being adenocarcinoma histology, also called renal cell cancers or renal cell carcinomas (RCCs).^1,2 The main histological types of RCC are clear cell, papillary, and chromophobe.^2,3 The prognosis of kidney cancer is relatively good if the tumor is diagnosed at an early stage and patients receive adequate treatment.^2-4 For patients with stage I-III tumors, upfront surgery is recommended as the primary curative treatment.^4,5 Surgery may consist of total removal of the kidney (i.e., complete or radical nephrectomy) or nephron-sparing surgery (i.e., partial nephrectomy).^6,7 Patients with high-risk clinical features may receive adjuvant immunotherapy or targeted therapy after surgery.^4,5,8,9 For patients with stage IV (i.e., metastatic) disease, surgery may be performed if medically able, but many patients may receive systemic therapy or be enrolled in clinical trials.^4,5,10

About 80-85% of kidney cancers are diagnosed at stages eligible for resection with presumably good prognosis.^1,2 Despite this, the burden of mortality falls disproportionally on different racial-ethnic groups in the U.S. Several population-based reports show that Black patients with kidney cancer experience worse survival than White patients, even when adjusted for stage.^11-18 The association between Hispanic ethnicity and survival is less studied, with some studies finding lower survival and others reporting no differences compared to non-Hispanic White patients.^13,18,19 Given the broad recommendations for surgical treatment of non-metastatic RCC and known improvement in survival associated with surgery,^2-4 its receipt is an important factor in studying racial-ethnic disparities in survival among patients with RCC. Evidence from U.S. population studies show that Black patients are less likely and Hispanic patients may be equally or more likely to receive surgery compared to non-Hispanic White patients with RCC.^{13,15,17,19-23} It is reasonable to conclude that racial differences in surgical treatment may partly explain racial disparities in survival in the U.S.

One factor that may influence both surgery receipt and survival and contribute to racial-ethnic disparities in RCC is access to care.^11-13 Studies have reported that patients with no or public health insurance are less likely to receive surgery and have worse survival than those with private health insurance.^11-13 Whether disparities in surgery and survival of RCC exist in equal access care settings is not well studied.^19,22,24,25 The current literature comes mainly from single-payer systems where members are required to enroll in the health plans to receive care, are geographically isolated, and may not include socioeconomic disadvantaged individuals.^19,22 Further study of surgery treatment and clinical outcomes among patients with RCC in geographically diverse equal-access healthcare settings is needed to better understand whether racial-ethnic disparities in kidney cancers may be mitigated by access to care or if other factors may be related to disparities.

The Department of Defense (DoD) beneficiary population provides an ideal setting to study possible racial-ethnic disparities in surgical treatment for RCC and in clinical outcomes in a patient population with equal access to medical care. The DoD provides medical care to over 9.6 million beneficiaries across the United States and abroad, including active-duty service members, activated National Guard and Reservists, retirees from military service, and their dependents through the Military Health System (MHS) and TRICARE benefit program.^26,27 Medical insurance and access to care is provided regardless of patient socioeconomic or demographic characteristics. Beneficiaries receive care with little to no out-of-pocket costs, and therefore, financial barriers to care are reduced compared to the general U.S. population.²⁸ This study aimed to compare receipt of surgical treatment, cancer recurrence, and all-cause death for patients with non-metastatic renal cell cancer between Non-Hispanic Black, Hispanic, and non-Hispanic White DoD beneficiaries with equal access to medical care in the MHS. We chose to focus the study on patients with non-metastatic disease for whom surgical intervention may be the primary treatment.^4,5

Materials and Methods

Data Sources

This retrospective cohort study used the Military Cancer Epidemiology (MilCanEpi) database, which contains information on patients diagnosed or treated for cancer in military treatment facilities of the MHS. The components of the MilCanEpi data and are discussed in detail elsewhere.²⁹ Briefly, the database contains patient and tumor information from the DoD Central Cancer Registry and DoD beneficiary eligibility and enrollment information and medical encounters for any condition in military treatment facilities or civilian facilities that was paid for by the DoD in the MHS Data Repository. The MilCanEpi database was approved for access for research by the Uniformed Services University of the Health Sciences Institutional Review Board, Bethesda, Maryland (FWA 00001628) on 19 July 2019 (Reference #914142) and renewed on 4 March 2025 (Reference #981045). The reporting of this study conforms to Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines.³⁰

Study Population

Eligible patients (n = 2145) included men and women age 18 or older who were newly diagnosed with a pathologically confirmed primary stage I, II, or III kidney cancer [International Classification of Diseases—Oncology, Third Edition (ICD-O-3) primary site code C64.9] with clear cell, papillary, chromophobe or unclassified renal cell carcinoma histology (ICD-O-3codes 80 323, 81 403, 82 603, 82 103, 82 703, 83 123, 83 163, 83 173, 83 203)¹⁴ between January 1, 1998 and December 31, 2014. Patients with stage IV (n = 328) RCC were excluded because surgery is not considered a primary treatment and many systemic therapies currently included in the guidelines were not available during the time period of our data (i.e., 1998-2014).^4,10 Patients with unknown stage tumors (n = 207) were also excluded due to inability to assess patients’ eligibility for surgical resection and presence of metastasis at diagnosis. Patients were included in the study if they were non-Hispanic Black or White races or Hispanic or Latinx ethnicity. Patients with other or unknown race-ethnicity were excluded due to uncertain racial-ethnic components and a small number of patients (n = 235).

Cancer Diagnosis and Treatment

Cancer diagnosis information included the date, tumor stage, and tumor grade retained from MilCanEpi. The pathologic diagnosis date from the cancer registry and the date of a first encounter for kidney cancer (ICD-9-CM 189.0) in the claims portion of the data were consolidated using systematic processes to determine diagnosis and its date.³¹ Tumor stage (I, II, or III) and grade (G1-4 or Gx) were summarized in the data using the American Joint Committee on Cancer (AJCC) system, 6^th or 7^th edition, based on the year of cancer diagnosis.^32,33 Information on surgery, radiation therapy, and chemotherapy initiated within 6 months of the cancer diagnosis date were obtained from the data. The period of 6 months was used to ascertain primary treatment to limit the inclusion of any treatment for cancer progression or metastasis. Surgery was further classified as partial, simple, or radical nephrectomy based on medical and billing codes (Supplemental Table 1). Local excision procedures or biopsy were not considered as primary surgical treatment. Although nephrectomy was considered the primary treatment for non-metastatic renal cell cancers and adjuvant treatment with either radiation or chemotherapy was not part of treatment guidelines for the years of our data (1998-2014),^10,34,35 we retained information on all treatment initiated within 6 months of the cancer diagnosis for consideration in the analysis. Treatment(s) and their date(s) were consolidated in the data using systematic procedures.³¹ Receipt of nephrectomy was considered a primary outcome for the study.

Clinical Outcomes

Information on clinical outcomes of cancer recurrence and all-cause death were determined in the data. Recurrence and its date were indicated by a record for diagnosis with secondary malignant neoplasm of the kidney (i.e., local recurrence, ICD-9-CM 198.0 or ICD-10-CM C79.00) or other sites (i.e., distant recurrence or metastasis) in the data occurring after the consolidated primary cancer diagnosis date through the end of the data.^36-38 To minimize the possibility of including secondary cancer that was present during initial diagnostic work-up or treatment planning, we also used an index date of either 60 days after cancer diagnosis (patients with no treatment) or 60 days after surgery (patients with treatment) for capturing recurrence and conducted a sensitivity analysis. Survival was determined from vital status and date of death in the data.

Other Study Variables

Information on patient sociodemographic variables were collected from the data, including age at cancer diagnosis, sex, race, ethnicity, marital status at diagnosis, active-duty military status, and military service branch. Comorbid medical conditions were summarized using the Elixhauser Index, modified for patients with cancer.^39,40 Conditions were included if a patient had at least 1 inpatient or 3 outpatient records with a diagnosis code occurring at least 30 days prior to the cancer diagnosis date. Care setting in the 6 months prior to and 6 months following cancer diagnosis were determined from patient records in the medical encounter data. Patients were classified as using military or civilian care based on the location of >80% of their medical encounters, including that for cancer diagnosis, treatment, and other care. If the 80% threshold was not met, they were classified as using “both” military and civilian care.

Statistical Analysis

We compared demographic and cancer diagnosis variables between non-Hispanic Black, Hispanic, and non-Hispanic White patients using frequency data and Chi-square statistics. Then, we evaluated the frequency of the study outcomes (i.e., nephrectomy, cancer recurrence, death) in the patient population. When outcome events occurred with low frequency (n < 11), cell suppression methods were used in the presentation of results to comply with the CMS Cell Suppression Policy.⁴¹ We used Poisson regression with log link and an offset for time-to-surgery to estimate the incidence rate ratios (IRRs) and 95% confidence intervals (CIs) for receiving nephrectomy in association with race-ethnicity using non-Hispanic White as the reference group. We performed the analysis for the study population overall and then stratified by tumor stage (I or II and III) and RCC histology subtype (clear cell, papillary, chromophobe, or unclassified) to assess any differences among patient subgroups. Then, we used Poisson regression to model the likelihood of receiving different surgery types (e.g., partial nephrectomy) between the racial-ethnic groups, both overall and in strata by tumor stage and histology when sample sizes allowed. Next, we used multivariable Cox proportional hazards regression models to estimate adjusted hazards ratios (AHRs) with 95% CIs for recurrence and all-cause death, respectively, in association with race-ethnicity using non-Hispanic White as the reference group. Follow-up time for Cox models was calculated as the time from cancer diagnosis to the date of the event (recurrence or death), last date of medical encounter in the data, or study end date on December 31, 2015, whichever occurred first. We assessed the data for overall associations and then stratified by tumor stage (all-cause death only) and histology. Multivariable Poisson and Cox regression models were adjusted for age at diagnosis, sex, marital status, active-duty military status, comorbidity, care setting, cancer diagnosis year, tumor stage, tumor histology, and tumor grade. Additionally, Cox models were adjusted for surgery treatment received as a time-dependent variable coded as 0 (no treatment) prior to surgery and 1 (treatment) at time of surgery to control for any effects of time-to-treatment on the outcomes. Chemotherapy and radiation were not adjusted for in Cox models due to very low frequency in the data (<1%). Results from regression models were considered statistically significant when the AIRR or AHR and 95% CIs did not include the null value of 1.00. Analyses were conducted in SAS 9.4 (SAS, Inc. Cary, NC).

Results

The study included 1371 non-Hispanic White, 362 non-Hispanic Black, and 177 Hispanic patients diagnosed with stage I-III RCC. The average age at diagnosis was 56.3 (SD +/− 13.2) years and 68.7% of patients were men. Comparing demographic and cancer diagnosis information between racial-ethnic groups (Table 1), a higher proportion of non-Hispanic Black patients were aged 40-49 or 50-59 and a lower proportion were aged 60-69 at diagnosis compared to Hispanic or non-Hispanic White patients; whereas a higher proportion of White patients were aged 70 or older at diagnosis compared to the other two racial-ethnic groups. Black patients had the lowest frequency of no comorbidity (38.1%), while the corresponding frequencies were 44.9% for White and 52.0% for Hispanic patients. There were no significant differences in sex, marital status, active-duty status, AJCC tumor stage, or AJCC tumor grade between the racial-ethnic groups (Table 1). The distribution of histology was different for Black patients relative to Hispanic or non-Hispanic White patients, such that a higher proportion of Black patients had papillary RCC and a lower proportion had clear cell RCC or unclassified RCC relative to the other racial-ethnic groups (Table 1).

Table 1.

Demographic and Tumor Information for Patients Diagnosed With Stage I-III Renal Cell Carcinoma by Race-Ethnicity in the U.S. Military Health System, 1998-2014.

Characteristic	Non-Hispanic White (N = 1371)	Non-Hispanic Black (N = 362)	Hispanic (N = 177)	P
Age at diagnosis	N (%)	N (%)	N (%)	<0.001
18-39	152 (11.1)	33 (9.1)	23 (13.0)
40-49	234 (17.1)	93 (25.7)	35 (19.8)
50-59	334 (24.4)	123 (34.0)	43 (24.3)
60-69	401 (29.2)	78 (21.5)	57 (32.2)
70+	250 (18.2)	35 (9.7)	19 (10.7)
Sex				0.14
Men	952 (69.4)	251 (69.3)	110 (62.1)
Women	419 (30.6)	111 (30.7)	67 (37.9)
Marital status				0.25
Married	1119 (81.6)	284 (78.5)	145 (81.9)
Single/sep/div/widowed	214 (15.6)	71 (19.6)	30 (16.9)
Unknown	38 (2.8)	7 (1.9)	2 (1.1)
Military active-duty status				0.98
No	1076 (78.5)	281 (77.6)	137 (77.4)
Yes	205 (15.0)	58 (16.0)	27 (15.3)
Unknown	90 (6.6)	23 (6.4)	13 (7.3)
Elixhauser comorbidity count				0.03
0	615 (44.9)	138 (38.1)	92 (52.0)
1-2	453 (33.0)	141 (39.0)	53 (29.9)
3+	303 (22.1)	83 (22.9)	32 (18.1)
AJCC tumor stage				0.05
I	1015 (74.0)	267 (73.8)	127 (71.8)
II	149 (10.9)	56 (15.5)	22 (12.4)
III	207 (15.1)	39 (10.8)	28 (15.8)
AJCC tumor grade				0.49
G1	204 (14.9)	48 (13.3)	22 (12.4)
G2	514 (37.5)	141 (39.0)	73 (41.2)
G3/4	300 (21.9)	66 (18.2)	39 (22.0)
Gx	353 (25.7)	107 (29.6)	43 (24.3)
Tumor histology subtype				<0.001
Renal cell carcinoma (RCC), unclassified	772 (56.3)	176 (48.6)	102 (57.6)
Clear cell (ccRCC)	405 (29.5)	75 (20.7)	55 (31.1)
Papillary (PRCC)	122 (8.9)	83 (22.9)	<11 (<6.2)
Chromophobe (ChRCC)	72 (5.3)	28 (7.7)	>11 (>6.2)
Care setting				0.02
Direct	908 (66.2)	257 (71.0)	127 (71.8)
Purchased care	126 (9.2)	19 (5.3)	18 (10.2)
Both	331 (24.1)	81 (22.3)	30 (16.9)
Unknown	6 (0.4)	5 (1.4)	2 (1.1)

AJCC, American Joint Committee on Cancer; NOS: not otherwise specified.

Regarding surgical treatment, overall, 89.1% of patients received a nephrectomy within 6 months of the cancer diagnosis: 58.5% received a complete nephrectomy and 30.6% received a partial nephrectomy. Among the racial-ethnic groups, overall, 86.7% of Black, 92.7%% of Hispanic, and 89.2% of White patients received a nephrectomy. In multivariable models adjusted for potential confounders, Black patients had a lower rate of nephrectomy (AIRR = 0.83, 95% CI = 0.72, 0.95), including both partial (AIRR = 0.68, 95% CI = 0.54, 0.85) and complete (AIRR = 0.82, 95% CI = 0.69, 0.97) nephrectomy, compared to non-Hispanic White patients. For Hispanic patients, there was no statistically significant difference in receipt of nephrectomy overall (AIRR = 1.16, 95% CI = 0.98, 1.37) compared to non-Hispanic White patients (Table 2). However, Hispanic patients had a higher rate of partial nephrectomy (AIRR = 1.45, 95% CI = 1.07, 1.96) and similar rate of complete nephrectomy compared to non-Hispanic White patients (Table 2).

Table 2.

Likelihood of Receiving Nephrectomy for Primary Surgical Treatment of Stage I-III Renal Cell Carcinoma by Race-Ethnicity in the Military Health System, 1998-2014.

	Non-Hispanic White (N = 1371)		Non-Hispanic Black (N = 362)			Hispanic (N = 177)
Nephrectomy receipt	N (%)	IRR (95%CI)	N (%)	IRR (95%CI)	AIRR (95% CI)^a	N (%)	IRR (95%CI)	AIRR (95% CI)^a
No	148 (10.8)	(Reference)	48 (13.3)	(Reference)	(Reference)	13 (7.3)	(Reference)	(Reference)
Yes^b	1223 (89.2)	1.00 (reference)	314 (86.7)	0.87 (0.77, 0.98)	0.83 (0.72, 0.95)	164 (92.7)	1.26 (1.07, 1.48)	1.16 (0.98, 1.37)

Nephrectomy type	N (%)	IRR (95%CI)	N (%)	IRR (95%CI)	AIRR (95% CI)^a	N (%)^e	IRR (95%CI)	AIRR (95% CI)^a
None	148 (10.8)	(Reference)	48 (13.3)	(Reference)	(Reference)	13 (7.3)	(Reference)	(Reference)
Partial nephrectomy	415 (30.3)	1.00 (reference)	111 (30.7)	0.86 (0.70, 1.07)	0.68 (0.54, 0.85)	58 (32.8)	1.42 (1.08, 1.87)	1.45 (1.07, 1.96)
Complete nephrectomy^c	808 (58.9)	1.00 (reference)	203 (56.1)	0.82 (0.70, 0.96)	0.82 (0.69, 0.97)	106 (59.9)	1.29 (1.05, 1.57)	1.13 (0.91, 1.40)

^aModel adjusted for age at diagnosis, sex, marital status, active-duty military status, care setting, comorbidity index, cancer diagnosis year, tumor histology, tumor stage, and tumor grade.

^bIncludes procedures for partial, simple, and radical nephrectomy.

^cIncludes procedures for simple and radical nephrectomy.

We further evaluated surgery receipt by tumor stage. Among 1409 patients with stage I RCC, there was a statistically significant lower rate for Black patients to receive nephrectomy (AIRR = 0.74, 95% CI = 0.64, 0.87), while Hispanic patients had a similar rate of nephrectomy compared to non-Hispanic White patients (Table 3). Regarding nephrectomy type, the rates of partial or complete nephrectomy relative to no treatment were significantly lower for Black patients compared to non-Hispanic White patients and there were no differences in nephrectomy type for Hispanic compared to White patients (data not shown), consistent with the overall results. Among 501 patients with stage II or III RCC, over 90% of patients received a nephrectomy. There were no statistically significant racial-ethnic differences in receiving nephrectomy for Black or Hispanic patients compared to White (Table 3), nor in the type of nephrectomy received (data not shown due to small sample size in some cells).

Table 3.

Comparison of Racial-Ethnic Groups in Nephrectomy Receipt by Tumor Stage for Patients Diagnosed With Renal Cell Carcinoma (RCC) in the Military Health System, 1998-2014.

Stage I RCC
	Non-Hispanic White (n = 1015)		Non-Hispanic Black (n = 267)			Hispanic (n = 127)
Nephrectomy receipt	N (%)	IRR (95%CI)	N (%)	IRR (95%CI)	AIRR (95% CI)^a	N (%)^b	IRR (95%CI)	AIRR (95% CI)^a
No	122 (12.0)	(Reference)	41 (15.4)	(Reference)	(Reference)	<11 (<8.7)	(Reference)	(Reference)
Yes^c	893 (88.0)	1.00 (reference)	226 (84.6)	0.81 (0.70, 0.94)	0.74 (0.64, 0.87)	>116 (>91.3)	1.36 (1.12, 1.65)	1.13 (0.92, 1.38)

Stage II or III RCC
	Non-Hispanic White (n = 356)		Non-Hispanic Black (n = 95)			Hispanic (n = 50)
	N (%)	IRR (95% CI)	N (%)^b	IRR (95% CI)	AIRR (95% CI)^a	N (%)^b	IRR (95% CI)	AIRR (95% CI)^a
No	26 (7.3)	(Reference)	<11 (<11.6)	(Reference)	(Reference)	<11 (<22)	(Reference)	(Reference)
Yes^c	330 (92.7)	1.00 (reference)	>84 (>88.2)	1.14 (0.90, 1.45)	1.02 (0.76, 1.36)	>39 (>78.0)	0.97 (0.71, 1.33)	0.75 (0.50, 1.10)

^aModel adjusted for age at diagnosis, sex, marital status, active-duty military status, care setting, comorbidity index, cancer diagnosis year, tumor grade and tumor histology subtype.

^bSome cells masked to comply with the CMS Cell Suppression Policy.

^cIncludes procedures for partial, simple, and radical nephrectomy.

We also assessed nephrectomy receipt by tumor histology subtype. Among 535 patients with clear cell RCC, Black patients had a statistically significantly lower rate (AIRR = 0.57, 95% CI = 0.42, 0.77) and Hispanic patients had a statistically higher rate (AIRR = 1.40, 95% CI = 1.01, 1.96) of receiving nephrectomy relative to non-Hispanic White patients (Table 4). Among patients with papillary carcinoma, there were no statistically significant differences in nephrectomy receipt (Table 4) between Black and non-Hispanic White patients. Associations among Hispanic patients were not calculated due to the low number of Hispanic patients with papillary carcinoma (n < 11). Among 1050 patients with unclassified RCC, there were no statistically significant racial-ethnic differences in receipt of nephrectomy (Table 4). In general, the results on nephrectomy type across the histologic subtypes were consistent with the overall results (data not shown). Analysis on surgery receipt and type for patients with chromophobe histology was not conducted due to few patients with the subtype.

Table 4.

Comparison of Racial-Ethnic Groups in Nephrectomy Receipt by Tumor Histology Subtype for Patients Diagnosed With Renal Cell Carcinoma (RCC) in the Military Health System, 1998-2014.

Clear cell RCC
Nephrectomy receipt	Non-Hispanic White (n = 405)		Non-Hispanic Black (n = 75)			Hispanic (n = 55)
	N (%)	IRR (95%CI)	N (%)	IRR (95%CI)	AIRR (95% CI)^a	N (%)^b	IRR (95%CI)	AIRR (95% CI)^a
No	47 (11.6)	(Reference)	14 (18.7)	(Reference)	(Reference)	<11 (<20.0)	(Reference)	(Reference)
Yes^c	358 (88.4)	1.00 (reference)	61 (81.3)	0.67 (0.51, 0.88)	0.57 (0.42, 0.77)	>44 (>80.0)	1.54 (1.15, 2.06)	1.40 (1.01, 1.96)

Papillary RCC
	Non-Hispanic White (n = 122)		Non-Hispanic Black (n = 83)			Hispanic (n < 11)
	N (%)^b	IRR (95% CI)	N (%)^b	IRR (95% CI)	AIRR (95% CI)^a	N (%)	IRR (95% CI)	AIRR (95% CI)^a
No	<11 (<9.0)	(Reference)	<11 (<13.3)	(Reference)	(Reference)	Did not calculate, total n < 11
Yes^c	>111 (>91.0)	1.00 (reference)	>72 (>86.7)	0.84 (0.63, 1.13)	1.17 (0.78, 1.75)	Did not calculate, total n < 11

Unclassified RCC
	Non-Hispanic White (n = 772)		Non-Hispanic Black (n = 176)			Hispanic (n = 102)
	N (%)	IRR (95% CI)	N (%)	IRR (95% CI)	AIRR (95% CI)^a	N (%)^b	IRR (95% CI)	AIRR (95% CI)^a
No	83 (10.8)	(Reference)	22 (12.5)	(Reference)	(Reference)	<11 (<10.8)	(Reference)	(Reference)
Yes^c	689 (89.2)	1.00 (reference)	154 (87.5)	0.87 (0.73, 1.03)	0.85 (0.70, 1.04)	>91 (>89.2)	1.08 (0.87, 1.34)	1.10 (0.87, 1.38)

^aModel adjusted for age at diagnosis, sex, marital status, active-duty military status, care setting, comorbidity index, cancer diagnosis year, tumor stage, and tumor grade.

^bSome cells masked to comply with the CMS Cell Suppression Policy.

^cIncludes procedures for partial, simple, and radical nephrectomy.

The median (IQR) follow-up for patients was 6.2 (3.2-10.2) years. Overall, 13.5% of patients experienced a cancer recurrence and about 9% of patients died. The frequency of recurrence was 8.6% for Black, 18.1% for Hispanic, and 14.2% for non-Hispanic White patients (Chi-square P = 0.003). In multivariable Cox models adjusted for potential confounders, Black patients had a statistically significant lower risk of recurrence (AHR = 0.61, 95% CI = 0.41, 0.92) while there was no difference for Hispanic (AHR = 1.08, 95% CI = 0.72, 1.64) compared to non-Hispanic White patients (Table 5). In the sensitivity analysis applying an index date of at least 60 days after diagnosis or treatment for capturing recurrence, we found similar results (data not shown). The frequency of death was 6.4% for Black, about 6.2% for Hispanic, and 9.9% for non-Hispanic White patients (Chi-square P = 0.014). The univariable model indicated a marginally lower risk of death for Black patients and a statistically lower risk of death for Hispanic patients relative to White (Table 5), but neither result was statistically significant in the multivariable model with adjustment for potential confounders and the association with Black race was notably attenuated.

Table 5.

Risk of Recurrence or All-Cause Death Expressed as Adjusted Hazard Ratios (AHRs) and 95% Confidence Intervals for Patients Diagnosed With Stage I-III Renal Cell Cancer in the U.S. Military Health System.

	Non-Hispanic White (N = 1371)			Non-Hispanic Black (N = 362)				Hispanic (N = 177)
Outcome	N (%)	Median time-to-event (months, IQR)^a	HR (95%CI)	N (%)	Median time-to-event (months, IQR)^a	HR (95%CI)	AHR (95%CI)^b	N (%)	Median time-to-event (months, IQR)^a	HR (95%CI)	AHR (95%CI)^b
Recurrence^c	195 (14.2)	35.1 (13.2, 79.8)	1.00 (reference)	31 (8.6)	36.8 (16.3, 78.6)	0.57 (0.39, 0.83)	0.61 (0.41, 0.92)	32 (18.1)	22.4 (11.2, 92.3)	1.24 (0.85, 1.80)	1.08 (0.72, 1.64)
All-cause death	136 (9.9)	26.7 (13, 46.3)	1.00 (reference)	23 (6.4)	21.3 (5.8, 42.9)	0.64 (0.41, 1.00)	0.88 (0.55, 1.40)	<11 (<6.2)	30 (21.2, 45.3)	0.43 (0.21, 0.88)	0.55 (0.27, 1.14)

^aTime between diagnosis and event (recurrence or death).

^bModel adjusted for age at diagnosis, sex, marital status, active-duty military status, care setting, comorbidity, cancer diagnosis year, tumor histology, tumor stage, tumor grade, and surgical treatment received (including nephrectomy, ablation, or local excision).

^cRecurrence captured in data by record with ICD-9 diagnosis code for secondary malignant neoplasm of the kidney or other organ sites.

We examined the data for possible racial-ethnic differences in the outcomes by tumor stage and histology when sample sizes and number of events were adequate. The low number of deaths among Hispanic patients precluded subgroup analysis by stage or histology for the outcome of overall survival. In the analysis by tumor stage, there was a tendency toward lower risk of recurrence for Black patients both among those with stage I (AHR = 0.64, 95% CI = 0.35, 1.19) and stage II or III tumors (AHR = 0.55, 95% CI = 0.31, 0.97) compared to White counterparts. The risks for recurrence among Hispanic patients were 1.38 (95% CI = 0.75, 2.54) among stage I and 0.81 (95% CI = 0.45, 1.45) among stage II or III. Regarding death, there were no significant differences for Black relative to White patients among those with stage I (AHR = 1.08, 95% CI = 0.60, 1.96) or stage II or III (AHR = 0.64, 95% CI = 0.29, 1.42) tumors. By histologic subtype, there was a lower risk of recurrence for Black patients with unspecified RCC (AHR = 0.43, 95% CI = 0.24, 0.77) and no difference for those with clear cell RCC (AHR = 1.18, 95% CI = 0.55, 2.51) compared to White patients. For Hispanic patients, the risk of recurrence was similar for those with unspecified RCC (AHR = 1.04, 95% CI = 0.64, 1.70) and elevated among those with clear cell RCC (AHR = 2.09, 95% CI = 0.87, 5.02). The number of events among those with papillary RCC was too small across the racial-ethnic groups to evaluate. Regarding death, there was no significant difference for Black patients among those with unspecified RCC (AHR = 1.00, 95% CI = 0.59, 1.72) and the number of events among Black patients with clear cell or papillary RCC were too small to evaluate.

Discussion

In the Military Health System, which provides access to care regardless of patient demographic or socioeconomic characteristics, a high proportion of patients received a nephrectomy for renal cell cancer, as recommended in the guidelines.^4,34 Nevertheless, we observed racial-ethnic differences in surgical management of RCC. Overall, Black patients had lower rates of nephrectomy than non-Hispanic White patients, with statistically significant findings among patients with stage I or clear cell RCC. However, Black patients had a tendency toward equal or better recurrence and survival outcomes compared to their non-Hispanic White counterparts, even for the patient subgroups by tumor stage and histology where differences in nephrectomy were found. On the other hand, Hispanic patients had higher rates of partial nephrectomy overall and had higher rates of surgery for those with clear cell RCC subtype. Additionally, Hispanic patients had a tendency toward better overall survival compared to non-Hispanic White patients with RCC. The similar or lower risk of outcomes for Black and Hispanic patients with RCC relative to non-Hispanic White patients contrasts observations in other national databases where patients had differential access to care.^{13,14,16,17,20,21} Our data suggests that when access to care is given and financial barriers to cancer treatment are minimized, racial and ethnic disparities in RCC outcomes may be reduced regardless of possible racial differences in nephrectomy for certain tumor stage and histologic groups.

Overall, 86.7% of Black patients with RCC in our study received nephrectomy, which is similar to rates reported from national databases covering a similar time period of our data.^13,17,20 In multivariable analysis, Black patients had a 17% lower rate of nephrectomy compared to non-Hispanic White patients. This included a significant 32% lower risk of partial nephrectomy and 18% lower risk of complete nephrectomy relative to no surgery. These findings are similar to those from studies of Surveillance Epidemiology and End Results (SEER) and National Cancer Database data covering a similar time period as our data.^13,17,20 The studies reported 18-32% lower odds of receiving nephrectomy, inclusive of both partial and complete nephrectomy, for Black compared to non-Hispanic White patients, when adjusting for patient, tumor, and socioeconomic factors.^13,17,20 Further analysis of surgery receipt by tumor stage and histologic subtype in our study of the MHS suggests that Black patients with Stage I or those with clear cell RCC had lower rates of nephrectomy than their non-Hispanic White counterparts. While the number of patients and low frequency of no surgery prohibited further analysis combining tumor stage and histology (e.g., stage I clear cell RCC) to examine racial-ethnic differences in surgery and surgery type as the study outcome, our analysis may provide some clues for future research in RCC disparities. The findings suggest that factors other than access to care may be related to surgery receipt.

Studies in equal access settings in which to draw comparisons are limited. One study of patients enrolled in the Northern California Kaiser Permanente, a single-payer healthcare organization, reported similar frequency of surgical treatment for kidney cancer between non-Hispanic Black and White patients.²² However, authors did not specify if the surgery was nephrectomy or if other procedures (e.g., ablation) were included and the likelihood of surgery was not assessed in a multivariable model. The results from our study in the nationwide MHS where patients have access and minimal financial barriers to care suggests that factors other than access to care may play a role in racial disparities in nephrectomy for patients with RCC. These factors are likely complex and multi-factorial and may include cognition and attitude toward cancer, health seeking behavior, or patient-provider communication.^42,43 These factors might also at least partially account for the observations from the national data in the general population. More research in equal access settings is needed to determine which factors may contribute to observed racial disparities in RCC treatment beyond access to care. Also, as surgical management of RCC shifts toward more conservative approaches,⁴⁴ future research is needed to determine whether there are racial-ethnic differences in the extent or appropriateness of surgery such as partial vs complete nephrectomy based on clinical presentation of the cancer.

Regarding ethnicity and treatment, our data showed no overall differences in nephrectomy between Hispanic and non-Hispanic White patients with RCC. However, Hispanic patients had a higher rate of nephrectomy among patients with clear cell RCC. Several population-based studies, where patients have varying access to care, also evaluated surgery among Hispanic patients with RCC and found that they were equally as likely as non-Hispanic White patients to receive nephrectomy overall, similar to the results of our present study.^13,20,21 In equal access settings, a study of patients with kidney cancer enrolled in Kaiser Permanente Northern California reported higher rates of surgery for Hispanic compared to non-Hispanic White patients, although surgery may have included ablation procedures and ethnicity was not evaluated in association with the likelihood of surgery in a multivariable model.¹⁹ Nevertheless, the results from studies in various U.S. healthcare settings as well as the data from the equal access MHS indicate that there may be no overall significant ethnic disparities in receiving nephrectomy. However, surgical extent may be another factor which should be considered. One study of patients in the general population reported that Hispanic patients were more likely to be undertreated, e.g., receiving partial nephrectomy when radical nephrectomy was indicated, compared to non-Hispanic White patients.²¹ In our present study, Hispanic patients had higher rates of partial nephrectomy and similar rates of complete nephrectomy relative to no surgery compared to non-Hispanic White patients overall. However, we did not have access to full clinical details and the number of patients was small for subgroup analysis by stage or histology. Thus, further research is needed to determine whether there are ethnic differences in surgical appropriateness or adherence to guideline recommended care based on tumor features and what impact any disparities may have on outcomes of RCC.

In this study of patients in the MHS diagnosed with RCC, Black patients had a lower risk of recurrence and similar risk of death compared to non-Hispanic White patients. The lower risk of recurrence was especially pronounced among those with unspecified histologic subtype of RCC. Additionally, there was no evidence of disparity in recurrence or survival outcomes between Black and non-Hispanic White patients among those with stage I or clear cell tumors, respectively, where differences in receipt of surgery were observed. While comparable data on recurrence risk from the general population is lacking, the overall finding of no racial difference in risk of death contrasts results from population studies in SEER and the National Cancer Database.^13,14,16,17 In the SEER data from 2005-2015, authors reported a 27% higher risk of all-cause mortality for Black compared to White patients when adjusted for socio-demographic, tumor, and treatment factors.¹⁷ A National Cancer Database study of patients diagnosed between 2004 and 2012 reported a more modest 9% increase in overall mortality for Black vs White patients.¹⁶ However, in equal access health systems, overall and disease-specific survival has been reported similar between non-Hispanic Black and White patients.^22,24 The reason for similar or better outcomes among Black patients in equal access systems despite the possible differences in surgical treatment received is unclear. It could be related to other health care access factors such as access to multidisciplinary medical teams, rehabilitation services, nutrition counseling, or other services which may improve outcomes. More research is needed to explore such hypotheses. Nevertheless, the results of our present study may suggest some effects of access to care on reducing racial disparities in survival observed in the general population.

Ethnic differences in kidney cancer outcomes and survival are less often reported in the literature than racial differences.^13,18,19,45 In our study, the overall risk of recurrence was similar and there was a trend toward lower risk of all-cause death for Hispanic patients with RCC compared to non-Hispanic White patients. However, the number of patients and events precluded any in-depth analysis. Evidence from other database and health system studies with varying levels of access to care point toward at least similar outcomes for Hispanic and non-Hispanic White patients, with one study reporting a 15% lower risk of all-cause death.^13,19,25 An earlier study of the Department of Defense cancer registry also showed no statistically significant difference in overall survival for Hispanic compared to non-Hispanic patients when equal access to care is provided.²⁵ Given the overall paucity of research on ethnic disparities in RCC, further studies are needed to evaluate whether there are differences in treatment and outcomes for ethnic minority patients with RCC in the U.S.

Our study uses a unique database to address possible racial-ethnic disparities in surgical treatment of RCC and outcomes of cancer recurrence and overall survival. However, there are several limitations to consider. First, the data available at the time of analysis included diagnoses between 1998 and 2014. Since then, adjuvant treatment with radiation or chemotherapy has been added the guidelines for renal cell cancers.^4,5 Because the treatments were not recommended during the time period of our data, and occurred with low frequency, we could not evaluate for any potential racial-ethnic differences in receipt of adjuvant therapy. Second, the overall frequency of nephrectomy in the study population was high (89%), which reduces statistical power for detecting differences in surgery receipt or surgery type between racial-ethnic groups. Likewise, the low number of patients without nephrectomy reduced study power for analysis stratified by tumor stage, tumor histology, or other subgroups (e.g., stage I clear cell RCC). Also, our study may be underpowered to detect significant differences in recurrence or death due to low numbers of patients and events by racial-ethnic group and the reliability of estimates may be reduced due to the presence of monotone likelihood.⁴⁶ Nevertheless, our study provides important information on treatment and outcomes of RCC in an equal access health system. Third, information on ethnicity may not be complete in the data and there is potential for misclassification where some Hispanic patients may be included in non-Hispanic racial groups. This may mask any true ethnic differences in the study outcomes, although the number of patients it affects may be too small to greatly affect our results. Next, the assessment of outcomes included recurrence as indicated by ICD-9 diagnosis codes in the medical encounter data and all-cause death from the cancer registry. We did not have clinical information to confirm recurrence and thus relied on published algorithms which may not accurately capture recurrence. Regarding death, information on cancer-specific death was not available in the data. Thus, we cannot rule out any possible racial and ethnic disparities in cancer-specific survival. Last, because of differences in patient populations and health system structures, the findings from the MHS may not be generalizable to other equal access health systems or to the general U.S. population.

Conclusions

Despite overall high rates of nephrectomy in the management of renal cell cancer in the equal access MHS, our data suggest that Black patients were less likely to receive nephrectomy than non-Hispanic White patients, especially among those with stage I tumors or clear cell histology. Nevertheless, Black patients experienced lower risk of recurrence and similar risk of all-cause death as non-Hispanic White patients with RCC that was consistent among the subgroups of patients where differences in surgery were noted. The results of our study support the role of access to care in reducing racial-ethnic disparities in cancer outcomes for non-Hispanic Black and Hispanic individuals observed in the general population, but also indicate that factors other than access to care may influence the receipt of surgery for Black patients. Future research using contemporary data sets in the age of targeted, personalized medicine and more conservative surgical approaches will be needed to address whether racial-ethnic disparities persist in treatment and outcomes of RCC and to identify factors related to any observed disparities.

Supplemental Material

Supplemental Material - Racial-Ethnic Comparisons in Surgical Treatment and Outcomes of Non-Metastatic Renal Cell Cancer in an Equal Access Health System

Supplemental Material for Racial-Ethnic Comparisons in Surgical Treatment and Outcomes of Non-Metastatic Renal Cell Cancer in an Equal Access Health System by Yvonne L. Eaglehouse, Sarah Darmon, Craig D. Shriver, and Kangmin Zhu in Cancer Control

Footnotes

Authors’ Note

The contents of this manuscript are the sole responsibility of the authors and do not necessarily reflect the views, assertions, opinions, or policies of the Uniformed Services University of the Health Sciences, the Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., the Department of Defense, or the Departments of the Army, Navy, or Air Force. Mention of trade names, commercial products, or organizations does not imply endorsement by the U.S. government.

Acknowledgements

The authors thank the Joint Pathology Center (JPC) for providing the Department of Defense (DoD) cancer registry data and the Defense Health Agency (DHA) for providing the Military Health System (MHS) data repository (MDR) data. The authors thank ICF International, the Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc. (HJF, Inc.), and the Uniformed Services University of the Health Sciences (USUHS) for data linkage and hosting.

ORCID iD

Yvonne L. Eaglehouse

Statements and Declarations

Author Contributions

YE, SD, and KZ were employees of the Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., a 501(c)(3) non-profit organization at the time the work was performed.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Murtha Cancer Center Research Program (MCCRP) of the Department of Surgery, Uniformed Services University of the Health Sciences (USUHS) under the auspices of the Henry M. Jackson Foundation for the Advancement of Military Medicine (HJF, Inc.), grant numbers HHU0001-16-2-0014 and HU0001-18-2-0032.

Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Data Availability Statement

The data that support the findings of this study are not publicly available due to the restrictions in the access and use of the MilCanEpi data specified in the data sharing agreements and regulatory approvals. The Department of Defense Central Cancer Registry (DoD CCR) data and data dictionary may be requested from the Joint Pathology Center and online at https://jpc.capmed.mil/. The Military Health System Data Repository (MDR) data and data dictionary may be requested from the Defense Health Agency and online at .

Supplemental Material

Supplemental material for this article is available online.

Appendix

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