Abstract
Studies have shown that whites have a higher colorectal cancer survival rate than blacks. However, it is unclear whether racial disparities result from unequal access to medical care or factors other than healthcare access or both. This study assessed whether non-Hispanic Whites (NHWs) and non-Hispanic Blacks (NHBs) differ in colon cancer (CC) survival in an equal-access healthcare system and examined whether racial differences varied by demographic and tumor characteristics. The study included 2,537 Military Health System patients diagnosed with CC between 1998 and 2007. Median follow-up time was 31.4 months. Cox models estimated hazard ratios (HR) and 95% confidence intervals (CI) for race, overall and stratified by age at diagnosis, sex, and tumor stage. No difference in overall survival (OS) between NHWs and NHBs was observed in general. However, among patients younger than 50 years old, NHBs experienced significantly worse OS than NHWs (HR: 2.27, 95% CI: 1.48–3.49). Further stratification by sex and tumor stage showed that this racial disparity was confined to women (HR: 2.80, 95% CI: 1.30–6.00) and patients with distant stage disease (HR: 2.65, 95% CI: 1.38–5.08) in this age group. When medical care is equally available to NHWs and NHBs, similar overall CC survival was observed; however, evidence of racial differences in survival was apparent for patients younger than 50 years old. This study suggests that factors other than access to care may be related to racial disparities in CC survival among younger, but not older, patients.
Keywords: race, colon cancer, survival, equal-access
Introduction
Colorectal cancer (CRC) is the third leading cause of cancer death among men and women in the United States (US), with an estimated 51,690 cause-specific deaths occurring in 2012 (1). Although CRC mortality rates have declined over the past three decades for both sexes, racial disparities have widened over time (1–4), with blacks experiencing higher mortality rates than whites (1, 3, 5, 6).
Among the general US population, studies have consistently shown that whites have a higher CRC survival rate compared to blacks (7–12). This racial disparity is due to multiple factors, the most influential likely being differences in disease presentation; blacks are more likely to be diagnosed with advanced CRCs than whites (5, 6). However, survival rates have been observed to be lower among blacks than whites, even after statistical adjustment for or stratification by tumor stage (10, 11), thus indicating the influence of other factors on survival.
Compared to whites, blacks are less likely to have health insurance coverage (13, 14) and regular access to physician care (15), which may partially account for the aforementioned disparities in disease presentation, and may also account for noted disparities in CRC prevention and treatment (16). Obtaining access to healthcare is a complex issue that depends on many socioeconomic factors, including education, income, employment status, and proximity to and utilization of healthcare facilities. However, because it’s difficult to fully adjust for socioeconomic status, it’s often unclear if racial differences that remain after adjustment (17, 18) are due to residual differences in healthcare access or other factors associated with CRC survival, such as biological factors that relate to genetic differences, tumor behavior or response to treatment, or cultural/behavioral factors that relate to the use of healthcare when access to care is available.
Examining survival in an equal-access system can help assess whether racial disparities are associated with unequal access to medical care or whether other factors, play a role in racial differences. Studies within the Veterans Affairs (VA) healthcare system, an ‘equal-access’ system that provides healthcare to veterans at little to no cost regardless of racial background, have observed similar CRC survival among white and black patients (19, 20). Similar to the VA system, the Department of Defense’s (DoD’s) Military Health System (MHS) also provides equal healthcare access, but to a larger beneficiary base, which includes both active duty and retired US military personnel and their dependents. Therefore, the MHS provides a unique opportunity to assess racial differences in CRC survival. A recent study within the MHS that examined the relationship of race and survival observed that blacks and whites have similar colon cancer (CC) survival (21). However, this study did not account for potential confounding by Hispanic ethnicity, medical comorbidities or tumor recurrence, and did not assess whether racial differences in survival varied by demographic or tumor characteristics.
Colon cancer constitutes almost three-fourths (72%) of incident CRC cases, of which a majority occur among whites and blacks in the US (1). The aim of the current study was to utilize data from both the cancer registry and the medical claims system of the MHS to further evaluate disparities in CC survival among Non-Hispanic Whites (NHWs) and Non-Hispanic Blacks (NHBs), while controlling for potential confounders such as comorbidities and cancer recurrence. Additionally, this study sought to assess whether any racial disparities in survival varied by age at diagnosis, sex, and tumor stage.
Materials & Method
Data source
Linked data from the DoD’s Central Cancer Registry (CCR) and the MHS Data Repository (MDR) were used in this study. Both data sources contain information on DoD beneficiaries, including active duty members, retirees, Guards and Reserve members and their dependents. CCR contains information on demographic, health, tumor characteristics, cancer treatment, recurrence, follow-up, and vital status from cancer cases diagnosed and/or treated at military treatment facilities (MTFs). The cancer registry conducts life-time follow-up on patients. CCR information is abstracted from patient medical records, reviewed, and entered into the database by certified cancer registrars. MDR contains administrative and medical care claims information (e.g., demographics, diagnoses, diagnostic and treatment procedures, prescriptions, and vital status) for both in-patient and out-patient services that are provided either directly at MTFs or at civilian facilities paid for by the DoD.
The Data Linkage project was reviewed and approved by the institutional review boards of the Walter Reed National Military Medical Center, Tricare Management Activity, and the National Cancer Institute Office of Human Subjects Research.
Study subjects
Patients who were diagnosed with CC between 1998 and 2007 with histologically confirmed, primary adenocarcinomas not reported via death certificate or autopsy were eligible for study inclusion (n=3,214). We excluded 644 persons who were not NHWs or NHBs, and 33 patients with missing survival information. Thus, the present analysis included 2,537 patients.
Study variables
Information on demographic characteristics was obtained from CCR. If data elements were unavailable from CCR, then missing values were supplemented from MDR. If values were missing from both data sources, the information was recorded as “unknown”. Demographic variables included age, sex, marital status, active duty status, and patient’s or sponsor’s military service branch and military rank at CC diagnosis. Tumor characteristics were obtained from CCR and included tumor grade, tumor stage, and primary colon cancer site. CCR and MDR data were combined to determine receipt of CC treatment (surgery, chemotherapy, or radiation therapy). If either data source indicated that treatment occurred within one year post-CC diagnosis, then receipt of treatment was classified as “yes”. Information on recurrence (yes/no) was obtained solely from CCR. The Charlson comorbidity index, not including CC diagnosis, was used to calculate the level of comorbidity for each patient (22). In order to reduce false diagnoses, comorbidities were considered present if a diagnosis was recorded at least three times in the MDR data during the year prior to CC diagnosis.
Statistical analysis
Differences in demographic, tumor, and health characteristics between NHW and NHB patients were compared using Chi-square tests. Cox models were used to estimate hazard ratios (HR) and 95% confidence intervals (CI) in order to assess the effect of race on CC survival while simultaneously adjusting for potential confounders. Racial differences in survival may vary by age at diagnosis, sex, and tumor stage (10, 12, 23); therefore, stratified analyses were conducted by these variables. Analyses by age was dichotomized at age 50 years to account for age-related differences in screening recommendations (24). The analytical outcome for this study was all-cause mortality, which was determined based on CCR and MDR data. Follow-up began at the date of CC diagnosis and was calculated through date of death or date of last contact. Follow-up was truncated at December 31, 2007. Length of follow-up ranged from 16 days to 119 months (median=31.4 months).
Statistical analyses were performed using Statistical Analysis System (SAS) software, Version 9.3 for Windows (SAS Institute, Inc., Cary, North Carolina). All tests of significance were two-tailed and performed at an alpha of 0.05.
Results
This study included 2,028 NHW and 509 NHB patients. Racial variation in demographic, tumor, and health characteristics were observed (Table 1). At the time of diagnosis, NHBs were younger and more likely than NHWs to be never married, active duty military service members, affiliated with the Army, and enlisted in the military (p≤0.03). Additionally, compared to NHWs, NHBs were more likely to be diagnosed with distant stage CC and cancers located in the splenic flexure or descending colon, and less likely to have cancer in the sigmoid colon (p≤0.01).
Table1.
Characteristics of Non-Hispanic White and Non-Hispanic Black patients with colon adenocarcinoma in the DoD military health system (N=2,537).
| Non-Hispanic White (n=2,028) |
Non-Hispanic Black (n=509) |
||||
|---|---|---|---|---|---|
| Characteristic | n | % | n | % | p-valuea |
| Age at diagnosis | |||||
| <50 years | 286 | 14 | 122 | 24 | <0.01 |
| 50–54 years | 204 | 10 | 66 | 13 | |
| 55–59 years | 259 | 13 | 65 | 13 | |
| 60–64 years | 373 | 18 | 93 | 18 | |
| 65–69 years | 230 | 11 | 67 | 13 | |
| 70–74 years | 228 | 11 | 45 | 9 | |
| 75–79 years | 196 | 10 | 30 | 6 | |
| 80+ years | 252 | 12 | 21 | 4 | |
| Sex | 0.86 | ||||
| Men | 1,244 | 61 | 310 | 61 | |
| Women | 784 | 39 | 199 | 39 | |
| Marital status at diagnosis | 0.03 | ||||
| Never married | 57 | 3 | 26 | 5 | |
| Married | 1,552 | 77 | 378 | 74 | |
| Other | 334 | 16 | 90 | 18 | |
| Unknown | 85 | 4 | 15 | 3 | |
| Active duty status at diagnosis | <0.01 | ||||
| No | 1,876 | 93 | 443 | 87 | |
| Yes | 152 | 7 | 66 | 13 | |
| Service branchb | <0.01 | ||||
| Army | 660 | 33 | 254 | 50 | |
| Air force | 683 | 34 | 130 | 26 | |
| Marines | 86 | 4 | 19 | 4 | |
| Navy | 469 | 23 | 80 | 16 | |
| Other | 22 | 1 | 4 | 1 | |
| Unknown | 108 | 5 | 22 | 4 | |
| Tumor stage | <0.01 | ||||
| Localized | 798 | 39 | 174 | 34 | |
| Regional | 856 | 42 | 210 | 41 | |
| Distant | 352 | 17 | 122 | 24 | |
| Unknown | 22 | 1 | 3 | 1 | |
| Tumor grade | 0.34 | ||||
| Well differentiated | 319 | 16 | 67 | 13 | |
| Moderately differentiated | 1,283 | 63 | 338 | 66 | |
| Poorly differentiated | 287 | 14 | 65 | 13 | |
| Unknown | 139 | 7 | 39 | 8 | |
| Colon cancer site | <0.01 | ||||
| Cecum | 433 | 21 | 115 | 23 | |
| Ascending colon | 398 | 20 | 95 | 19 | |
| Hepactic flexure | 101 | 5 | 25 | 5 | |
| Transverse colon | 163 | 8 | 47 | 9 | |
| Splenic flexure | 67 | 3 | 34 | 7 | |
| Descending colon | 130 | 6 | 51 | 10 | |
| Sigmoid colon | 686 | 34 | 129 | 25 | |
| Unknown/Colon, NOS | 50 | 2 | 13 | 3 | |
| Comorbiditiesc | 0.18 | ||||
| None | 1,205 | 59 | 325 | 64 | |
| One | 272 | 13 | 63 | 12 | |
| Two or more | 551 | 27 | 121 | 24 | |
2-sided p-value.
Service branch of active duty member or sponsor.
Charlson comorbidity index. Colon cancer was not included in calculation.
During multivariate analysis, no racial differences in overall survival (OS) were observed (Table2: HR: 1.02, 95% CI: 0.86–1.21). Stratified analysis by sex and tumor stage yielded similar results. However, evidence of effect modification by age was apparent. Among patients aged 50 years or older, no racial difference in survival was observed; however, among younger patients, mortality was twice as high for NHBs than NHWs (HR: 2.03, 95% CI: 1.30–3.19).
Table2.
Multivariate analysis assessing the effect of race on colon cancer survival among 2,537 DoD beneficiaries with colon adenocarcinoma, overall and stratified by age, sex, and tumor stage.
| Number of patients |
|||||
|---|---|---|---|---|---|
| Strata | Alive | Dead | Hrab | 95% CI | |
| Overall | |||||
| Non-Hispanic White | 1,315 | 713 | 1.00 | reference | |
| Non-Hispanic Black | 325 | 184 | 1.05 | 0.89 | 1.24 |
| Age | |||||
| <50 years | |||||
| Non-Hispanic White | 213 | 73 | 1.00 | reference | |
| Non-Hispanic Black | 74 | 48 | 2.27 | 1.48 | 3.49 |
| ≥ 50 years | |||||
| Non-Hispanic White | 1,102 | 640 | 1.00 | reference | |
| Non-Hispanic Black | 251 | 136 | 0.85 | 0.70 | 1.02 |
| Sex | |||||
| Men | |||||
| Non-Hispanic White | 786 | 458 | 1.00 | reference | |
| Non-Hispanic Black | 196 | 114 | 1.08 | 0.87 | 1.35 |
| Women | |||||
| Non-Hispanic White | 529 | 255 | 1.00 | reference | |
| Non-Hispanic Black | 129 | 70 | 1.01 | 0.76 | 1.34 |
| Stage | |||||
| Local | |||||
| Non-Hispanic White | 656 | 142 | 1.00 | reference | |
| Non-Hispanic Black | 156 | 18 | 1.03 | 0.61 | 1.76 |
| Regional | |||||
| Non-Hispanic White | 580 | 276 | 1.00 | reference | |
| Non-Hispanic Black | 145 | 65 | 1.08 | 0.81 | 1.43 |
| Distant | |||||
| Non-Hispanic White | 70 | 282 | 1.00 | reference | |
| Non-Hispanic Black | 22 | 100 | 0.96 | 0.75 | 1.24 |
Hazard ratio (HR) and 95% confidence intervals (CI).
Models were adjusted for year at diagnosis, age at diagnosis, race, sex, marital status at diagnosis, active duty status at diagnosis, sponsor's service branch, tumor stage, tumor grade, colon cancer site, comorbidities, recurrence, surgery, chemotherapy, and radiation therapy. Stratified variables were not included in stratified analysis.
Table 3 shows the results further stratified by age-sex and age-tumor stage. Although mortality risk was elevated among younger NHB men and women, only NHB women had a significantly worse survival than their white counterparts (HR: 2.87, 95% CI: 1.35–6.11). Additionally, among younger patients with distant stage disease, mortality was significantly worse for NHBs compared to NHWs (HR: 2.45, 95% CI: 1.15–5.22).
Table3.
Multivariate analysis assessing the effect of race on colon cancer survival among 2,537 DoD beneficiaries with colon adenocarcinoma, stratified by age-sex and age-tumor stage.
| Age | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| <50 years (n=408) | ≥ 50 years (n=2,129) | |||||||||
| Number of patients |
Number of patients |
|||||||||
| Alive | Dead | Hrab | 95% CI | Alive | Dead | Hrab | 95% CI | |||
| Sex | ||||||||||
| Men | ||||||||||
| Non-Hispanic White | 123 | 33 | 1.00 | reference | 663 | 425 | 1.00 | reference | ||
| Non-Hispanic Black | 45 | 24 | 1.68 | 0.82 | 3.45 | 151 | 90 | 0.85 | 0.67 | 1.08 |
| Women | ||||||||||
| Non-Hispanic White | 90 | 40 | 1.00 | reference | 439 | 215 | 1.00 | reference | ||
| Non-Hispanic Black | 29 | 24 | 2.80 | 1.30 | 6.00 | 100 | 46 | 0.81 | 0.57 | 1.14 |
| Tumor stage | ||||||||||
| Local | ||||||||||
| Non-Hispanic White | 78 | 3 | 1.00 | reference | 578 | 139 | 1.00 | reference | ||
| Non-Hispanic Black | 34 | 2 | --c | --c | --c | 122 | 16 | 0.89 | 0.52 | 1.54 |
| Regional | ||||||||||
| Non-Hispanic White | 114 | 28 | 1.00 | reference | 466 | 248 | 1.00 | reference | ||
| Non-Hispanic Black | 37 | 14 | 1.79 | 0.67 | 4.79 | 108 | 51 | 0.83 | 0.61 | 1.14 |
| Distant | ||||||||||
| Non-Hispanic White | 21 | 42 | 1.00 | reference | 49 | 240 | 1.00 | reference | ||
| Non-Hispanic Black | 3 | 32 | 2.65 | 1.38 | 5.08 | 19 | 68 | 0.77 | 0.57 | 1.04 |
Hazard ratio (HR) and 95% confidence intervals (CI).
Models were adjusted for year at diagnosis, age at diagnosis, race, sex, marital status at diagnosis, active duty status at diagnosis, sponsor's service branch, tumor stage, tumor grade, colon cancer site, comorbidities, recurrence, surgery, chemotherapy, and radiation therapy. Stratified variables were not included in stratified analysis.
The model had too few deaths to converge, therefore data was unavailable.
Discussion
This study shows no overall difference in OS between NHWs and NHBs in the MHS, an equal-access healthcare system. This is similar to what was found among patients in the VA healthcare system and a previous analysis within the MHS (19–21). However, there were indications of effect modification by age; among patients younger than 50 years of age, NHBs experienced significantly worse survival than NHWs. Further stratification by sex and tumor stage showed that this racial disparity was confined to women and patients with distant stage disease below the age of 50 years.
Our findings appear to indicate that among older individuals, but not younger individuals, having equal access to healthcare results in similar CC survival among NHWs and NHBs. A recent study among individuals in the general US population aged 50 years and older estimated that approximately 20% of the black-white disparity in CRC mortality rates could be attributed to racial differences in screening, which are related to access to health care (25). In the current study, when access to screening is seemingly equal, no racial difference in survival was observed among individuals for whom screening is recommended (patients ≥ 50 years of age), suggesting that equal access to healthcare may play an even larger role than previously estimated.
Among younger patients for whom screening is typically not recommended, racial variation in CC survival within our equal access system implies that factors beyond access to care may contribute to the racial disparity. However, it’s unclear why racial disparities were found primarily in younger women and younger patients with distant cancer stage. It’s possible that the age-related racial variations seen in this study are due to differences in knowledge, attitudes, and behavior towards diagnosis or the use of medical care such as treatment amongst NHWs and NHBs. However, to the best of our knowledge, research is limited in this area and, therefore, further population-based outcomes research is warranted.
This study had several strengths. Namely, the possible confounding effects of multiple factors including Hispanic ethnicity, medical comorbidities, and tumor recurrence were simultaneously controlled for and effect modification by age at diagnosis, sex, and tumor stage were assessed using detailed, linked electronic cancer registry and medical claims data. Limitations were also present. Sample sizes were limited for certain stratified analyses. For example, there were small numbers of patients with localized or regional cancer among those aged younger than 50 years. This prevented us from ascertaining whether decreased survival among blacks was truly specific to distant tumors only. All-cause mortality, not disease-specific mortality, was the outcome of this study; therefore, it’s possible that the inclusion of non-CC deaths may have affected our results. However, the impact on our results is likely minimal, particularly among older individuals. Only if other causes of death were less common among NHBs than NHWs, which is unlikely, could the inclusion of all-cause mortality have obscured a true difference in cause-specific mortality among older individuals. It’s harder to rule out the possibility that the racial disparity in survival among the young was not driven by racial differences in other causes of death. However, given that no significant difference in comorbidity was observed between NHWs and NHBs, even after stratifying by age (data not shown), the likelihood that other causes of death influenced any racial differences seen in this study is minimal.
In a healthcare system where medical care is equally available to NHWs and NHBs, similar OS in patients with CC was observed. However, there was evidence of racial differences in survival by age. Thus, it’s possible that factors other than equal-access to care influence racial disparities in OS among younger, but not older, patients with CC.
Acknowledgements
This project was supported by John P. Murtha Cancer Center, Walter Reed National Military Medical Center via the Uniformed Services University of the Health Sciences under the auspices of the Henry M. Jackson Foundation for the Advancement of Military Medicine and by the intramural research program of the National Cancer Institute. The original data linkage was supported by the United States Military Cancer Institute (USMCI) and Division of Cancer Epidemiology and Genetics (DCEG), National Cancer Institute. The authors thank the following individuals and institutes for their contributions to or support for the original data linkage project: Mr. Guy J. Garnett, Mr. David E. Radune, and Dr. Aliza Fink of ICF Macro; Ms. Wendy Funk, Ms. Julie Anne Mutersbaugh, Ms. Linda Cottrell, and Ms. Laura Hopkins of Kennel and Associates, Inc.; Ms. Kim Frazier, Dr. Elder Granger, and Dr. Thomas V. Williams of TMA; Ms. Annette Anderson, Dr. Patrice Robinson, and Dr. Chris Owner of the Armed Forces Institute of Pathology; Dr. Joseph F. Fraumeni, Jr., Dr. Robert N. Hoover, Dr. Susan S. Devesa and Ms. Gloria Gridley of NCI; Dr. John Potter, Mr. Raul Parra, Ms. Anna Smith, Ms. Fiona Renalds, Mr. William Mahr, Mrs. Hongyu Wu, Dr. Larry Maxwell, Mr. Miguel Buddle, and Ms.Virginia Van Horn of USMCI.
Footnotes
Publisher's Disclaimer: Disclaimers:
The views expressed in this article are those of the author and do not necessarily reflect the official policy or position of the Department of the Navy, Army, Department of Defense, National Cancer Institute, nor the U.S. Government. Nothing in the presentation implies any Federal/DOD/DOA/DON endorsement.
Conflict of interest: The authors declare that there is no conflict of interest.
References
- 1.American Cancer Society. Colorectal Cancer Facts & Figures 2011–2013. Atlanta: American Cancer Society; 2011. [Google Scholar]
- 2.Wingo PA, Cardinez CJ, Landis SH, Greenlee RT, Ries LA, Anderson RN, et al. Long-term trends in cancer mortality in the United States, 1930–1998. Cancer. 2003;97(12 Suppl):3133–3275. doi: 10.1002/cncr.11380. [DOI] [PubMed] [Google Scholar]
- 3.DeLancey JO, Thun MJ, Jemal A, Ward EM. Recent trends in Black-White disparities in cancer mortality. Cancer Epidemiol Biomarkers Prev. 2008;17(11):2908–2912. doi: 10.1158/1055-9965.EPI-08-0131. [DOI] [PubMed] [Google Scholar]
- 4.Robbins AS, Siegel RL, Jemal A. Racial Disparities in Stage-Specific Colorectal Cancer Mortality Rates From 1985 to 2008. J Clin Oncol. 2012;30(4):401–405. doi: 10.1200/JCO.2011.37.5527. [DOI] [PubMed] [Google Scholar]
- 5.Polite BN, Dignam JJ, Olopade OI. Colorectal cancer and race: understanding the differences in outcomes between African Americans and whites. Med Clin North Am. 2005;89(4):771–793. doi: 10.1016/j.mcna.2005.03.001. [DOI] [PubMed] [Google Scholar]
- 6.Polite BN, Dignam JJ, Olopade OI. Colorectal cancer model of health disparities: understanding mortality differences in minority populations. J Clin Oncol. 2006;24(14):2179–2187. doi: 10.1200/JCO.2005.05.4775. [DOI] [PubMed] [Google Scholar]
- 7.Wingo PA, Ries LA, Parker SL, Heath CW., Jr Long-term cancer patient survival in the United States. Cancer Epidemiol Biomarkers Prev. 1998;7(4):271–282. [PubMed] [Google Scholar]
- 8.Merrill RM, Henson DE, Ries LA. Conditional survival estimates in 34,963 patients with invasive carcinoma of the colon. Dis Colon Rectum. 1998;41(9):1097–1106. doi: 10.1007/BF02239430. [DOI] [PubMed] [Google Scholar]
- 9.Clegg LX, Li FP, Hankey BF, Chu K, Edwards BK. Cancer survival among US whites and minorities: a SEER (Surveillance, Epidemiology, and End Results) Program population-based study. Arch Intern Med. 2002;162(17):1985–1993. doi: 10.1001/archinte.162.17.1985. [DOI] [PubMed] [Google Scholar]
- 10.Mayberry RM, Coates RJ, Hill HA, Click LA, Chen VW, Austin DF, et al. Determinants of black/white differences in colon cancer survival. J Natl Cancer Inst. 1995;87(22):1686–1693. doi: 10.1093/jnci/87.22.1686. [DOI] [PubMed] [Google Scholar]
- 11.Hashiguchi Y, Hase K, Ueno H, Shinto E, Naito Y, Kajiwara Y, et al. Impact of race/ethnicity on prognosis in patients who underwent surgery for colon cancer: analysis for white, african, and East asian americans. Ann Surg Oncol. 2012;19(5):1517–1528. doi: 10.1245/s10434-011-2113-5. [DOI] [PubMed] [Google Scholar]
- 12.Marcella S, Miller JE. Racial differences in colorectal cancer mortality. The importance of stage and socioeconomic status. J Clin Epidemiol. 2001;54(4):359–366. doi: 10.1016/s0895-4356(00)00316-4. [DOI] [PubMed] [Google Scholar]
- 13.Kirby JB, Kaneda T. Unhealthy and uninsured: exploring racial differences in health and health insurance coverage using a life table approach. Demography. 2010;47(4):1035–1051. doi: 10.1007/BF03213738. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Ward E, Halpern M, Schrag N, Cokkinides V, DeSantis C, Bandi P, et al. Association of insurance with cancer care utilization and outcomes. CA Cancer J Clin. 2008;58(1):9–31. doi: 10.3322/CA.2007.0011. [DOI] [PubMed] [Google Scholar]
- 15.Mahmoudi E, Jensen GA. Diverging racial and ethnic disparities in access to physician care: comparing 2000 and 2007. Med Care. 2012;50(4):327–334. doi: 10.1097/MLR.0b013e318245a111. [DOI] [PubMed] [Google Scholar]
- 16.Demissie K, Oluwole OO, Balasubramanian BA, Osinubi OO, August D, Rhoads GG. Racial differences in the treatment of colorectal cancer: a comparison of surgical and radiation therapy between Whites and Blacks. Ann Epidemiol. 2004;14(3):215–221. doi: 10.1016/j.annepidem.2003.08.002. [DOI] [PubMed] [Google Scholar]
- 17.Du XL, Fang S, Vernon SW, El-Serag H, Shih YT, Davila J, et al. Racial disparities and socioeconomic status in association with survival in a large population-based cohort of elderly patients with colon cancer. Cancer. 2007;110(3):660–669. doi: 10.1002/cncr.22826. [DOI] [PubMed] [Google Scholar]
- 18.Du XL, Meyer TE, Franzini L. Meta-analysis of racial disparities in survival in association with socioeconomic status among men and women with colon cancer. Cancer. 2007;109(11):2161–2170. doi: 10.1002/cncr.22664. [DOI] [PubMed] [Google Scholar]
- 19.Dominitz JA, Samsa GP, Landsman P, Provenzale D. Race, treatment, and survival among colorectal carcinoma patients in an equal-access medical system. Cancer. 1998;82(12):2312–2320. doi: 10.1002/(sici)1097-0142(19980615)82:12<2312::aid-cncr3>3.0.co;2-u. [DOI] [PubMed] [Google Scholar]
- 20.Robinson CN, Balentine CJ, Marshall CL, Anaya DA, Artinyan A, Awad SA, et al. Ethnic disparities are reduced in VA colon cancer patients. Am J Surg. 2010;200(5):636–639. doi: 10.1016/j.amjsurg.2010.07.020. [DOI] [PubMed] [Google Scholar]
- 21.Hofmann LJ, Lee S, Waddell B, Davis KG. Effect of race on colon cancer treatment and outcomes in the Department of Defense healthcare system. Dis Colon Rectum. 2010;53(1):9–15. doi: 10.1007/DCR.0b013e3181bdcdb2. [DOI] [PubMed] [Google Scholar]
- 22.Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40(5):373–383. doi: 10.1016/0021-9681(87)90171-8. [DOI] [PubMed] [Google Scholar]
- 23.Hendifar A, Yang D, Lenz F, Lurje G, Pohl A, Lenz C, et al. Gender disparities in metastatic colorectal cancer survival. Clin Cancer Res. 2009;15(20):6391–6397. doi: 10.1158/1078-0432.CCR-09-0877. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.U.S. Preventive Services Task Force. Rockville, MD: Agency for Healthcare Research and Quality; 2008. Oct, Screening for Colorectal Cancer: U.S. Preventive Services Task Force Recommendation Statement. External Web Site Icon AHRQ Publication 08-05124-EF-3. [Google Scholar]
- 25.Lansdorp-Vogelaar I, Kuntz KM, Knudsen AB, van Ballegooijen M, Zauber AG, Jemal A. Contribution of screening and survival differences to racial disparities in colorectal cancer rates. Cancer Epidemiol Biomarkers Prev. 2012;21(5):728–736. doi: 10.1158/1055-9965.EPI-12-0023. [DOI] [PMC free article] [PubMed] [Google Scholar]