Abstract
Background:
Race and income are social factors that contribute to persistent inequities in cancer care delivery/outcomes. However, cancer disparities patterns within underserved populations—such as those with annual household income (AHI)<$15,000—remain incompletely understood. We evaluated survival among low-income Americans who identified as Black or White with breast, prostate, lung, or colorectal cancer.
Methods:
Using the Southern Community Cohort Study prospectively-collected data and linkages to state cancer registries and National Death Index, we identified adults with primary breast, prostate, lung or colorectal cancer. Cox proportional hazards models were used to compare race-specific overall survival among individuals by AHI.
Results:
A total of 4,651 individuals who self-identified as Black or White were diagnosed with breast (n=1,223), prostate (n=1,158), lung (n=1,469) or colorectal (n=801) cancer. Over half (56.8%) reported AHI<$15,000. Specific to those reporting AHI<$15,000, Black individuals with lung cancer had a significantly lower hazard of death than Whites after adjustment for age, sex, surgery, clinical stage, smoking history, lung cancer subtype, BMI, COPD, persistent poverty, enrollment year and source (HR=0.78; 95%CI=0.66–0.92). In contrast, Black females with AHI<$15,000 had a slightly higher hazard of death than Whites for breast cancer (HR=1.20; 95%CI=0.85–1.70), although these differences were not statistically significant. No racial differences were observed for prostate or colorectal cancers.
Conclusions:
Among individuals with AHI<$15,000, racial disparities in survival were observed for lung, but not other, cancers.
Impact:
Disentangling the interplay of race and individual-level income on cancer survival guides improved access to high-quality cancer care services, which could reduce inequities and improve clinical outcomes.
Keywords: colorectal cancer, lung, breast, prostate, disparities, income, socioeconomic survival
INTRODUCTION
In 2025, it is projected that over 2 million new invasive cancer cases will occur in the United States—for which cancers of the breast, prostate, lung/bronchus and colorectum will cumulatively account for nearly 50% of these events.(1) Despite the wealth of studies undertaken across these common cancer types to improve clinical care and outcomes, survival differences persist across populations by race and socioeconomic status.(2) It is well-established that individuals who identify as Black and those with lower socioeconomic status experience poorer survival after a cancer diagnosis. Indeed, a recent study by Moss and colleagues found that counties with at least one-fifth of residents living in poverty for over two decades had elevated mortality rates for all cancer types.(3) These persistent poverty counties, which clustered in the Southeastern United States and had higher percentages of Black residents compared with other counties, were reported to have a 12% higher cancer mortality. Yet our current understanding into the complex interplay of these social determinants of health on cancer development and outcomes—specifically among these populations experiencing a disproportionate cancer burden—remains incompletely understood.
The place-based inequities that individuals who are living in areas with higher poverty experience when diagnosed with cancer pervade through the cancer care continuum: cancer incidence rates are higher, including for late-stage disease; delays in cancer diagnosis, in access to cancer treatment and in treatment initiation are more common; and deviations to guideline-concordant care occur more frequently.(4–6) Together, these factors yield poorer survival outcomes.(7) When studying poverty and cancer health disparities, population-based and other prior studies—including those utilizing cancer registry data from the National Cancer Institute’s Surveillance, Epidemiology and End Results (SEER) Program, have largely focused on area-based (e.g., county, zip code) attributes of poverty and income.(8–10) Yet, the federal determination of poverty measures is based on individual-level income, including household income. Therefore, the study of annual household income (AHI) and cancer survival in the Southeastern United States is essential to disentangle this constellation of social determinants of health among underserved populations and to direct appropriate resources that will contribute to improving patient outcomes. Herein, we investigated survival patterns among 4,651 low-income individuals ages 45 years and older diagnosed with breast, prostate, lung or colorectal cancers in the Southern Community Cohort Study.
METHODS
Southern Community Cohort Study (SCCS)
The SCCS is a prospective cohort established for research investigations focused on health disparities in cancer and other chronic diseases.(11) From 2002 to 2009, approximately 85,000 adults aged 45+ years were recruited across 12 states in the Southeastern US (Alabama, Arkansas, Florida, Georgia, Kentucky, Louisiana, Mississippi, North Carolina, South Carolina, Tennessee, Virginia, and West Virginia). A total of 86% of SCCS participants were recruited at 71 Federally Qualified Health Centers (FQHC) and other Community Health Centers (CHCs) that primarily provide primary healthcare services to underserved populations. The SCCS protocol was approved by the Vanderbilt University Medical Center and Meharry Medical College Institutional Review Board and all participants provided written informed consent. The study was conducted in accordance with the ethical principles of the Declaration of Helsinki.
Data Sources and Collection
At study enrollment, participants completed a baseline questionnaire to provide information on social and demographic characteristics, including self-identified race and sex, and annual household income (AHI), lifestyle characteristics (e.g., smoking history) and medical history (e.g., chronic obstructive pulmonary disease [COPD]; colonoscopy; prostate-specific antigen [PSA] test for males; mammogram and menopausal status for females). Data on primary cancer diagnosis, surgical resection, tumor characteristics, American Joint Committee on Cancer (AJCC) clinical stage and outcomes were ascertained via linkages to state registries and the National Death Index. Persistent poverty was defined using the U.S. Department of Agriculture’s Economic Research Service (ERS) and National Cancer Institute Census tract information based on whether enrollment was in an area where ≥20% of the population were living in poverty in the 1990 and 2000 decennial censuses, as well as in the 2007–2011 and 2015–2019 American Community Survey (ACS) 5-year estimates. Incident colorectal cancer was defined by ICD-O codes C18.0, C18.2-C18.9, C19.9 and C20.9, incident breast cancer in females by ICD-O codes C50.X, incident prostate cancer in males by ICD-O codes C61.X, and incident lung cancers by ICD-O codes C34.X. For breast cancer subtypes, information on estrogen receptor (ER), progesterone receptor (PR) and human epidermal growth factor receptor 2 (HER2) status were abstracted from state cancer registry records and supplemented by pathology reports and medical records as previously described.(12) Lung cancer subtypes were defined by ICD-O histology codes.
Statistical Analysis
Baseline characteristics by AHI level (<$15,000/$15,000+) across cancer types were compared using chi-square and t-tests for categorical and continuous variables, respectively. Multivariable Cox proportional hazards regression models were calculated to estimate hazard ratios (HRs) and 95% confidence intervals (CI) for overall and cancer-specific mortality. Follow-up time was calculated as the total years from enrollment date to death date or censoring (e.g., loss to follow-up, latest follow-up). All models were adjusted for age at cancer diagnosis (years), enrollment source (CHCs/general population), time between study enrollment and cancer diagnosis (years), self-identified race (White/Black), persistent poverty (yes/no), surgical resection (yes/no), AJCC stage, smoking history (non-smoker, current/former smoker), body mass index (kg/m2) and COPD (yes/no). Data missingness was handled with the multivariate imputation by chained equations (MICE) algorithm. Additional co-variates in cancer-specific models included: cancer subtype (Luminal A/B, HER2, Triple negative), mammogram (never, ever) and menopausal status (pre-menopausal, post-menopausal) for female breast cancer; PSA test (never, ever) for prostate cancer; tumor subtype (adenocarcinoma, squamous cell, small cell, large cell, other) and sex (male, female) for lung cancer; tumor site (colon, rectosigmoid junction/rectum), colonoscopy (never, ever) and sex for colorectal cancer. Stratified and sensitivity analyses were also conducted by AHI level. Data were analyzed using R statistical software (version 4.3.2). All statistical tests were two-sided, and statistical significance was defined with P<0.05.
RESULTS
A total of 4,651 individuals enrolled in the SCCS who were subsequently diagnosed with a primary breast, prostate, lung or colorectal cancer during the follow-up were included in this study—of whom 56.8% (n=2,644) reported an AHI less than $15,000 (Table 1). Across all cancers, individuals who reported an AHI less than $15,000 had a statistically significantly higher proportion of the population who resided in areas of persistent poverty (54.2% vs 36.0%, respectively; P<0.01). Notably, among the individuals who reported an AHI of at least $15,000, 81.0% (n=1,626 of 2,007) reported an AHI less than $50,000.
Table 1.
Summary of sociodemographic and clinical characteristics by annual household income (AHI) for 4,651 individuals diagnosed with a primary breast, prostate, lung and colorectal cancer: Southern Community Cohort Study (SCCS).
| Characteristic | Study Population (N=4,651) | AHI <$15,000 (N=2,644) | AHI $15,000+ (N=2,007) | P |
|---|---|---|---|---|
| Self-identified Race | <0.01 | |||
| White | 1336 (28.7) | 677 (25.6) | 659 (32.8) | |
| Black | 3315 (71.3) | 1967 (74.4) | 1348 (67.2) | |
| Sex | <0.01 | |||
| Male | 2216 (47.6) | 1192 (45.1) | 1024 (51.0) | |
| Female | 2435 (52.4) | 1452 (54.9) | 983 (49.0) | |
| Age at Cancer Diagnosis | ||||
| Years, Mean (std) | 62.3 (8.5) | 62.1 (8.8) | 62.5 (8.2) | 0.17 |
| Annual Household Income (AHI) | - | |||
| <$15,000 | 2644 (56.8) | 2644 (100.0) | - | |
| $15,000–$24,999 | 968 (20.8) | - | 968 (48.2) | |
| $25,000–$49,999 | 658 (14.1) | - | 658 (32.8) | |
| $50,000+ | 381 (8.2) | - | 381 (19.0) | |
| Persistent Poverty | <0.01 | |||
| No | 2495 (53.6) | 1210 (45.8) | 1285 (64.0) | |
| Yes | 2156 (46.4) | 1434 (54.2) | 722 (36.0) | |
| Smoking History | <0.01 | |||
| Non-smoker | 1292 (27.8) | 617 (23.3) | 675 (33.6) | |
| Former smoker | 1165 (25.0) | 573 (21.7) | 592 (29.5) | |
| Current smoker | 2194 (47.2) | 1454 (55.0) | 740 (36.9) | |
| Body Mass Index | ||||
| kg/m2, Mean (std) | 29.4 (7.2) | 29.2 (7.6) | 29.7 (6.7) | 0.01 |
| Chronic obstructive pulmonary disease (COPD) | <0.01 | |||
| No | 4149 (89.2) | 2300 (87.0) | 1849 (92.1) | |
| Yes | 502 (10.8) | 344 (13.0) | 158 (7.9) | |
| Surgical Resection | <0.01 | |||
| None | 2184 (47.0) | 1356 (51.3) | 828 (41.3) | |
| Yes | 2467 (53.0) | 1288 (48.7) | 1179 (58.7) | |
| AJCC Stage | <0.01 | |||
| I | 835 (18.0) | 444 (16.8) | 391 (19.5) | |
| II | 1159 (24.9) | 568 (21.5) | 591 (29.4) | |
| III | 615 (13.2) | 382 (14.4) | 233 (11.6) | |
| IV | 822 (17.7) | 546 (20.7) | 276 (13.8) | |
| Unknown/Unstaged | 1220 (26.2) | 704 (26.6) | 516 (25.7) | |
| Primary Cancer Site | <0.01 | |||
| Breast | 1223 (26.3) | 669 (25.3) | 554 (27.6) | |
| Prostate | 1158 (24.9) | 528 (20.0) | 630 (31.4) | |
| Lung | 1469 (31.6) | 986 (37.3) | 483 (24.1) | |
| Colorectum | 801 (17.2) | 461 (17.4) | 340 (16.9) |
Note: Estimates are presented as No (%) unless otherwise specified. Abbreviations: AHI, annual household income; std, standard deviation. P-value calculations do not include unknown values.
Approximately half of the study population was comprised of females (52.4%; n=2,435) (Table 1). Mean age at cancer diagnosis was 62.1 years (std, 8.8 years) among individuals with an AHI less than $15,000 and 62.5 years (std, 8.2 years) among individuals with an AHI of at least $15,000. Across all cancer types, individuals who identified as Black and individuals who were current smokers comprised a greater proportion of the population with an AHI less than $15,000 (all P<0.01). Females comprised a larger proportion of the population who reported an AHI less than $15,000 (P<0.01). For clinical and tumor characteristics, individuals with an AHI less than $15,000 had a lower proportion of cases who underwent surgical resection of the primary tumor (AHI <$15,000: 48.7% vs AHI $15,000+: 58.7%; P<0.01). AJCC clinical stage varied by income level, with a higher proportion of individuals diagnosed with stage IV disease among the group reporting an AHI less than $15,000 (20.7% vs 13.8%, respectively; P<0.01). The overall mortality rates for individuals diagnosed with female breast, prostate or colorectal cancer in the SCCS was below 50% over the study period (breast: 26.5%, prostate: 26.0%, and colorectal: 46.3%) (Tables 1 and 2). For individuals diagnosed with lung cancer in this cohort, the overall mortality rate was 79.2%. Cancer-specific mortality rates were 15.3% for female breast cancer, 8.1% for prostate cancer, 30.6% for colorectal cancer and 66.8% for lung cancer (Table 1 and Supplementary Table 1).
Table 2.
Adjusted hazard of overall death for individuals with a primary breast, prostate, colorectal and lung cancer by annual household income (AHI) level: Southern Community Cohort Study.
| All cases | Annual Household Income (AHI) |
|||||||
|---|---|---|---|---|---|---|---|---|
| <$15,000 | $15,000+ | |||||||
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| Observational Study Estimate | HR (95% CI)* | P | Deaths | HR (95% CI)* | P | Deaths | HR (95% CI)* | P |
| (A) Breast Cancer | ||||||||
| Race | ||||||||
| White | 1.0 (Ref) | 56 | 1.0 (Ref) | 39 | 1.0 (Ref) | |||
| Black | 1.14 (0.87, 1.49) | 0.35 | 162 | 1.20 (0.85, 1.70) | 0.30 | 67 | 0.95 (0.60, 1.49) | 0.81 |
| Age at Cancer Diagnosis | ||||||||
| Years | 1.04 (1.03, 1.06) | <0.01 | 218 | 1.04 (1.02, 1.05) | <0.01 | 106 | 1.06 (1.04, 1.09) | <0.01 |
| Surgical Resection | ||||||||
| None | 1.0 (Ref) | 45 | 1.0 (Ref) | 15 | 1.0 (Ref) | |||
| Yes | 0.31 (0.23, 0.43) | <0.01 | 173 | 0.26 (0.18, 0.39) | <0.01 | 91 | 0.34 (0.18, 0.64) | <0.01 |
| AJCC Stage | ||||||||
| I | 1.0 (Ref) | 41 | 1.0 (Ref) | 17 | 1.0 (Ref) | |||
| II | 2.01 (1.43, 2.82) | <0.01 | 55 | 1.73 (1.13, 2.64) | 0.01 | 33 | 2.91 (1.59, 5.31) | <0.01 |
| III | 4.45 (3.13, 6.32) | <0.01 | 56 | 3.64 (2.37, 5.59) | <0.01 | 26 | 8.11 (4.24, 15.50) | <0.01 |
| IV | 10.02 (6.44, 15.58) | <0.01 | 28 | 6.94 (4.05, 11.91) | <0.01 | 12 | 22.66 (10.10, 50.86) | <0.01 |
| Breast Cancer Subtype | ||||||||
| Luminal A | 1.0 (Ref) | 118 | 1.0 (Ref) | 64 | 1.0 (Ref) | |||
| Luminal B | 1.11 (0.77, 1.61) | 0.58 | 27 | 1.06 (0.67, 1.67) | 0.81 | 10 | 1.21 (0.61, 2.43) | 0.59 |
| HER2 | 1.36 (0.89, 2.09) | 0.15 | 20 | 1.24 (0.75, 2.04) | 0.40 | <10 | 1.75 (0.74, 4.18) | 0.21 |
| Triple negative | 1.37 (1.04, 1.80) | 0.03 | 53 | 1.30 (0.93, 1.81) | 0.13 | 26 | 1.58 (0.95, 2.62) | 0.08 |
| Menopausal Status | ||||||||
| Post-Menopausal | 1.0 (Ref) | 206 | 1.0 (Ref) | 100 | 1.0 (Ref) | |||
| Pre-Menopausal | 1.31 (0.77, 2.24) | 0.32 | 12 | 0.88 (0.46, 1.69) | 0.71 | <10 | 5.67 (2.13, 15.08) | <0.01 |
| Persistent Poverty | ||||||||
| No | 1.0 (Ref) | 120 | 1.0 (Ref) | 68 | 1.0 (Ref) | |||
| Yes | 0.99 (0.78, 1.27) | 0.95 | 98 | 0.97 (0.72, 1.31) | 0.84 | 38 | 1.15 (0.73, 1.80) | 0.55 |
| Smoking History | ||||||||
| Never smoker | 1.0 (Ref) | 89 | 1.0 (Ref) | 55 | 1.0 (Ref) | |||
| Former smoker | 1.14 (0.86, 1.51) | 0.37 | 51 | 1.05 (0.73, 1.51) | 0.79 | 31 | 1.30 (0.82, 2.05) | 0.26 |
| Current smoker | 1.18 (0.90, 1.55) | 0.24 | 78 | 1.23 (0.89, 1.71) | 0.21 | 20 | 1.07 (0.63, 1.83) | 0.80 |
| Body Mass Index | ||||||||
| kg/m2 | 1.00 (0.99, 1.02) | 0.78 | 218 | 1.01 (0.99, 1.02) | 0.52 | 106 | 1.00 (0.97, 1.03) | 0.85 |
| COPD | ||||||||
| No | 1.0 (Ref) | 218 | 1.0 (Ref) | 106 | 1.0 (Ref) | |||
| Yes | 1.08 (0.76, 1.54) | 0.66 | 26 | 0.86 (0.56, 1.33) | 0.50 | 13 | 2.22 (1.21, 4.10) | 0.01 |
| Mammogram** | ||||||||
| Never | 1.0 (Ref) | 28 | 1.0 (Ref) | 12 | 1.0 (Ref) | |||
| Ever | 0.78 (0.54, 1.12) | 0.18 | 190 | 0.89 (0.57, 1.38) | 0.61 | 94 | 0.72 (0.38, 1.39) | 0.33 |
| AHI Level | ||||||||
| $15,000+ | 1.0 (Ref) | |||||||
| <$15,000 | 1.52 (1.18, 1.95) | <0.01 | ||||||
| (B) Prostate Cancer | ||||||||
| Race | ||||||||
| White | 1.0 (Ref) | 22 | 1.0 (Ref) | 25 | 1.0 (Ref) | |||
| Black | 1.19 (0.84, 1.69) | 0.33 | 155 | 0.97 (0.60, 1.57) | 0.90 | 99 | 1.32 (0.76, 2.27) | 0.33 |
| Age at Cancer Diagnosis | ||||||||
| Years | 1.06 (1.04, 1.07) | <0.01 | 177 | 1.06 (1.04, 1.08) | <0.01 | 124 | 1.06 (1.02, 1.09) | <0.01 |
| Surgical Resection | ||||||||
| None | 1.0 (Ref) | 127 | 1.0 (Ref) | 87 | 1.0 (Ref) | |||
| Yes | 0.69 (0.53, 0.90) | 0.01 | 50 | 0.76 (0.53, 1.08) | 0.13 | 37 | 0.62 (0.41, 0.96) | 0.03 |
| AJCC Stage | ||||||||
| I | 1.0 (Ref) | 10 | 1.0 (Ref) | <10 | 1.0 (Ref) | |||
| II | 1.26 (0.77, 2.05) | 0.35 | 87 | 1.17 (0.60, 2.30) | 0.64 | 75 | 1.32 (0.65, 2.70) | 0.44 |
| III | 1.36 (0.64, 2.89) | 0.42 | <10 | 1.39 (0.49, 3.96) | 0.53 | <10 | 1.41 (0.47, 4.19) | 0.54 |
| IV | 6.58 (3.76, 11.52) | <0.01 | 34 | 5.47 (2.62, 11.40) | <0.01 | 14 | 9.40 (3.78, 23.41) | <0.01 |
| Persistent Poverty | ||||||||
| No | 1.0 (Ref) | 70 | 1.0 (Ref) | 77 | 1.0 (Ref) | |||
| Yes | 0.94 (0.73, 1.19) | 0.59 | 107 | 1.05 (0.76, 1.45) | 0.78 | 47 | 0.71 (0.48, 1.06) | 0.09 |
| Smoking History | ||||||||
| Never smoker | 1.0 (Ref) | 29 | 1.0 (Ref) | 24 | 1.0 (Ref) | |||
| Former smoker | 1.32 (0.93, 1.87) | 0.12 | 43 | 0.88 (0.53, 1.44) | 0.60 | 44 | 1.85 (1.11, 3.10) | 0.02 |
| Current smoker | 2.28 (1.62, 3.20) | <0.01 | 105 | 1.67 (1.07, 2.61) | 0.02 | 56 | 3.21 (1.88, 5.48) | <0.01 |
| Body Mass Index | ||||||||
| kg/m2 | 1.01 (0.99, 1.03) | 0.34 | 177 | 0.99 (0.96, 1.01) | 0.32 | 124 | 1.05 (1.02, 1.09) | <0.01 |
| COPD | ||||||||
| No | 1.0 (Ref) | 164 | 1.0 (Ref) | 117 | 1.0 (Ref) | |||
| Yes | 1.15 (0.72, 1.82) | 0.57 | 13 | 0.99 (0.56, 1.77) | 0.98 | <10 | 1.67 (0.75, 3.71) | 0.21 |
| Prostate-Specific Antigen (PSA) Test** | ||||||||
| Never | 1.0 (Ref) | 81 | 1.0 (Ref) | 36 | 1.0 (Ref) | |||
| Ever | 0.93 (0.72, 1.20) | 0.57 | 96 | 1.06 (0.77, 1.45) | 0.74 | 88 | 0.78 (0.51, 1.17) | 0.23 |
| AHI Level | ||||||||
| $15,000+ | 1.0 (Ref) | |||||||
| <$15,000 | 1.29 (1.00, 1.67) | 0.05 | ||||||
| (C) Lung Cancer | ||||||||
| Race | ||||||||
| White | 1.0 (Ref) | 278 | 1.0 (Ref) | 147 | 1.0 (Ref) | |||
| Black | 0.85 (0.74, 0.97) | 0.02 | 530 | 0.78 (0.66, 0.92) | <0.01 | 208 | 1.07 (0.84, 1.38) | 0.58 |
| Age at Cancer Diagnosis | ||||||||
| Years | 1.01 (1.01, 1.02) | <0.01 | 808 | 1.02 (1.01, 1.02) | <0.01 | 355 | 1.02 (1.00, 1.03) | 0.02 |
| Sex | ||||||||
| Female | 1.0 (Ref) | 429 | 1.0 (Ref) | 185 | 1.0 (Ref) | |||
| Male | 0.87 (0.77, 0.98) | 0.03 | 379 | 0.87 (0.75, 1.01) | 0.07 | 170 | 0.83 (0.66, 1.05) | 0.12 |
| Surgical Resection | ||||||||
| None | 1.0 (Ref) | 727 | 1.0 (Ref) | 321 | 1.0 (Ref) | |||
| Yes | 0.39 (0.31, 0.48) | <0.01 | 81 | 0.39 (0.30, 0.51) | <0.01 | 34 | 0.36 (0.24, 0.54) | <0.01 |
| AJCC Stage | ||||||||
| I | 1.0 (Ref) | 78 | 1.0 (Ref) | 26 | 1.0 (Ref) | |||
| II | 1.57 (1.15, 2.15) | 0.01 | 43 | 1.56 (1.08, 2.28) | 0.02 | 20 | 1.71 (0.95, 3.08) | 0.08 |
| III | 1.67 (1.30, 2.13) | <0.01 | 165 | 1.61 (1.21, 2.16) | <0.01 | 66 | 1.80 (1.10, 2.92) | 0.02 |
| IV | 3.48 (2.76, 4.40) | <0.01 | 367 | 3.27 (2.48, 4.29) | <0.01 | 172 | 4.26 (2.69, 6.76) | <0.01 |
| Lung Cancer Subtype | ||||||||
| Adenocarcinoma | 1.0 (Ref) | 283 | 1.0 (Ref) | 116 | 1.0 (Ref) | |||
| Squamous cell | 1.07 (0.91, 1.27) | 0.39 | 169 | 1.05 (0.86, 1.28) | 0.66 | 76 | 1.16 (0.86, 1.57) | 0.33 |
| Small cell | 1.30 (1.09, 1.57) | <0.01 | 132 | 1.35 (1.09, 1.68) | 0.01 | 53 | 1.28 (0.91, 1.82) | 0.16 |
| Large cell | 1.60 (1.14, 2.25) | 0.01 | 25 | 1.86 (1.22, 2.82) | <0.01 | 13 | 1.29 (0.71, 2.32) | 0.41 |
| Other | 1.12 (0.96, 1.31) | 0.15 | 199 | 1.11 (0.92, 1.34) | 0.29 | 97 | 1.23 (0.92, 1.64) | 0.16 |
| Persistent Poverty | ||||||||
| No | 1.0 (Ref) | 369 | 1.0 (Ref) | 223 | 1.0 (Ref) | |||
| Yes | 1.11 (0.98, 1.26) | 0.10 | 439 | 1.14 (0.98, 1.33) | 0.08 | 132 | 1.01 (0.79, 1.27) | 0.97 |
| Smoking History | ||||||||
| Never smoker | 1.0 (Ref) | 33 | 1.0 (Ref) | 18 | 1.0 (Ref) | |||
| Former smoker | 1.03 (0.75, 1.41) | 0.87 | 138 | 0.97 (0.66, 1.44) | 0.89 | 77 | 1.10 (0.64, 1.88) | 0.74 |
| Current smoker | 1.23 (0.91, 1.66) | 0.17 | 637 | 1.24 (0.86, 1.80) | 0.25 | 260 | 1.21 (0.73, 2.01) | 0.47 |
| Body Mass Index | ||||||||
| kg/m2 | 0.99 (0.98, 1.00) | 0.11 | 808 | 1.00 (0.99, 1.01) | 0.93 | 355 | 0.97 (0.95, 0.99) | <0.01 |
| COPD | ||||||||
| No | 1.0 (Ref) | 667 | 1.0 (Ref) | 306 | 1.0 (Ref) | |||
| Yes | 1.15 (0.98, 1.35) | 0.09 | 141 | 1.14 (0.94, 1.38) | 0.19 | 49 | 1.15 (0.84, 1.57) | 0.39 |
| AHI Level | ||||||||
| $15,000+ | 1.0 (Ref) | |||||||
| <$15,000 | 1.21 (1.05, 1.38) | 0.01 | ||||||
| (D) Colorectal Cancer | ||||||||
| Race | ||||||||
| White | 1.0 (Ref) | 49 | 1.0 (Ref) | 39 | 1.0 (Ref) | |||
| Black | 1.13 (0.87, 1.46) | 0.37 | 180 | 1.10 (0.78, 1.56) | 0.60 | 103 | 1.22 (0.81, 1.84) | 0.33 |
| Age at Cancer Diagnosis | ||||||||
| Years | 1.03 (1.01, 1.04) | <0.01 | 229 | 1.04 (1.02, 1.06) | <0.01 | 142 | 1.02 (1.00, 1.04) | 0.12 |
| Sex | ||||||||
| Female | 1.0 (Ref) | 93 | 1.0 (Ref) | 77 | 1.0 (Ref) | |||
| Male | 0.76 (0.60, 0.95) | 0.02 | 136 | 0.89 (0.66, 1.21) | 0.46 | 65 | 0.59 (0.41, 0.85) | <0.01 |
| Surgical Resection | ||||||||
| None | 1.0 (Ref) | 74 | 1.0 (Ref) | 31 | 1.0 (Ref) | |||
| Yes | 0.32 (0.24, 0.41) | <0.01 | 155 | 0.33 (0.24, 0.46) | <0.01 | 111 | 0.24 (0.15, 0.39) | <0.01 |
| AJCC Stage | ||||||||
| I | 1.0 (Ref) | 30 | 1.0 (Ref) | 15 | 1.0 (Ref) | |||
| II | 1.76 (1.17, 2.63) | 0.01 | 27 | 1.51 (0.89, 2.56) | 0.13 | 26 | 2.57 (1.33, 4.94) | 0.01 |
| III | 2.42 (1.65, 3.55) | <0.01 | 48 | 2.75 (1.71, 4.42) | <0.01 | 20 | 2.26 (1.14, 4.47) | 0.02 |
| IV | 8.42 (5.86, 12.10) | <0.01 | 78 | 7.28 (4.57, 11.62) | <0.01 | 54 | 12.51 (6.72, 23.30) | <0.01 |
| Tumor Site | ||||||||
| Colon | 1.0 (Ref) | 162 | 1.0 (Ref) | 113 | 1.0 (Ref) | |||
| Rectosigmoid Junction/Rectum | 0.80 (0.62, 1.03) | 0.09 | 65 | 1.07 (0.78, 1.46) | 0.69 | 27 | 0.49 (0.31, 0.77) | <0.01 |
| Persistent Poverty | ||||||||
| No | 1.0 (Ref) | 101 | 1.0 (Ref) | 89 | 1.0 (Ref) | |||
| Yes | 0.92 (0.74, 1.16) | 0.49 | 128 | 0.88 (0.66, 1.17) | 0.37 | 53 | 0.90 (0.62, 1.31) | 0.59 |
| Smoking History | ||||||||
| Never smoker | 1.0 (Ref) | 79 | 1.0 (Ref) | 60 | 1.0 (Ref) | |||
| Former smoker | 0.95 (0.73, 1.24) | 0.70 | 60 | 0.94 (0.66, 1.35) | 0.75 | 41 | 0.86 (0.56, 1.32) | 0.48 |
| Current smoker | 1.12 (0.85, 1.46) | 0.42 | 90 | 1.51 (1.06, 2.16) | 0.02 | 41 | 0.81 (0.52, 1.26) | 0.35 |
| Body Mass Index | ||||||||
| kg/m2 | 1.00 (0.99, 1.02) | 0.69 | 229 | 1.01 (0.99, 1.04) | 0.18 | 142 | 0.99 (0.96, 1.01) | 0.30 |
| COPD | ||||||||
| No | 1.0 (Ref) | 201 | 1.0 (Ref) | 131 | 1.0 (Ref) | |||
| Yes | 1.25 (0.88, 1.80) | 0.22 | 28 | 0.98 (0.64, 1.51) | 0.93 | 11 | 1.87 (0.95, 3.68) | 0.07 |
| Colonoscopy** | ||||||||
| Never | 1.0 (Ref) | 176 | 1.0 (Ref) | 102 | 1.0 (Ref) | |||
| Ever | 1.01 (0.79, 1.30) | 0.94 | 53 | 1.00 (0.72, 1.39) | 0.99 | 40 | 1.03 (0.66, 1.58) | 0.91 |
| AHI Level | ||||||||
| $15,000+ | 1.0 (Ref) | |||||||
| <$15,000 | 1.26 (1.00, 1.59) | 0.05 | ||||||
Breast cancer models were adjusted for enrollment source, years between study enrollment and cancer diagnosis, age, race, surgery, stage, smoking history, body mass index, COPD, mammogram, persistent poverty, breast cancer subtype and menopausal status. Prostate cancer models were adjusted for: enrollment source, years between study enrollment and cancer diagnosis, race, age, surgery, stage, smoking history, body mass index, COPD, prostate-specific antigen test, and persistent poverty. Lung cancer models were adjusted for: enrollment source, years between study enrollment and cancer diagnosis, race, age, sex, surgery, stage, smoking history, body mass index, COPD, persistent poverty, and lung cancer subtype. Colorectal cancer models were adjusted for: enrollment source, years between study enrollment and cancer diagnosis, age, sex, race, surgery, stage, smoking history, body mass index, COPD, colonoscopy, persistent poverty, and tumor site, as appropriate.
Screening test history at time of study enrollment.
To unravel the complex interplay of race and income on outcomes across these four common cancer types, we characterized overall survival patterns by AHI (Figure 1 and Table 2). For lung and breast cancers, individuals with an AHI less than $15,000 had a statistically significantly increased hazard of overall death compared to those with higher AHI after adjusting for clinical, individual and demographic factors (Lung cancer: HR 1.21, 95%CI 1.05–1.38, P=0.01; Breast cancer: HR 1.52, 95%CI 1.18–1.95, P<0.01) (Table 2). Similar patterns were observed with AHI level for cancer-specific survival in lung and breast cancers, although these results did not reach the threshold for statistical significance (Lung cancer: HR 1.16, 95%CI 1.00–1.34, P=0.05; Breast cancer: HR 1.21, 95%CI 0.88–1.68, P=0.24) (Supplementary Table 1).
Figure 1.
Adjusted survival curves by annual household income (AHI) level and self-identified race across four common cancer types: (A) breast cancer, (B) prostate cancer, (C) lung/bronchus cancer, and (D) colorectal cancer.
No apparent overall or cancer-specific survival differences were observed by race for breast, prostate or colorectal cancer cases in adjusted models. In contrast, those who identified as Black diagnosed with lung cancer had a 15% decreased hazard of overall death and 22% decreased hazard of cancer-specific death compared to White counterparts after adjustment for enrollment source, years between study enrollment and cancer diagnosis, age, sex, surgery, AJCC stage, smoking history, body mass index, COPD, AHI level, persistent poverty and lung cancer subtype (Overall death: HR 0.85, 95%CI 0.74–0.97, P=0.02; Cancer-specific death: HR 0.85, 95%CI 0.73–0.99, P=0.03) (Table 2 and Supplementary Table 1).
To deepen our understanding of these observed racial differences in lung cancer survival, we stratified cases by AHI level (Table 2c and Supplementary Table 1c). No racial differences in overall or cancer-specific survival were observed among individuals with an AHI of at least $15,000 for lung cancer (Black vs White: Overall HR 1.07, 95%CI 0.84–1.38; P=0.58; Cancer-specific HR 1.04, 95%CI 0.79–1.36, P=0.78). However, among those with an AHI less than $15,000, racial disparities in survival persisted among individuals with lung cancer, as those who identified as Black had a 22% reduced hazard of death compared with Whites in adjusted models (Overall HR 0.78, 95%CI 0.66–0.92, P<0.01; Cancer-specific HR 0.78, 95%CI 0.65–0.93, P=0.01). Notably, among individuals diagnosed with lung cancer who reported an AHI less than $15,000, the population of individuals who identified as Black was comprised of a higher proportion of non-smokers (5.5% vs 2.1%, respectively; P<0.01), presented more frequently with lung cancer adenocarcinomas (41.0% vs 31.5%, respectively; P<0.01), and more frequently resided in areas of persistent poverty (67.5% vs 25.2%, respectively; P<0.001) versus Whites (Supplementary Table 2). To also disentangle the individual-level and place-level contributors of racial differences in lung cancer survival, we also examined associations between persistent poverty and overall death by race and AHI level. As presented in Table 3, we observed that only among individuals who identified as Black and reported an AHI less than $15,000, those residing in persistent poverty areas had a 28% increased hazard of overall death compared with those who did not reside in areas where ≥20% of the population were living in poverty (HR 1.28, 95%CI 1.06–1.55, P=0.01).
Table 3.
Associations between persistent poverty and overall death by annual household income (AHI) level and self-identified race for individuals with a primary breast, prostate, colorectal and lung cancer: Southern Community Cohort Study.
| Estimates of persistent poverty | Annual Household Income (AHI) |
|||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| <$15,000 |
$15,000+ |
|||||||||||
| Black |
White |
Black |
White |
|||||||||
| Deaths | HR (95% CI)* | P | Deaths | HR (95% CI)* | P | Deaths | HR (95% CI)* | P | Deaths | HR (95% CI)* | P | |
| Breast Cancer | ||||||||||||
| No | 71 | 1.0 (Ref) | 49 | 1.0 (Ref) | 33 | 1.0 (Ref) | 35 | 1.0 (Ref) | ||||
| Yes | 91 | 1.07 (0.77, 1.50) | 0.68 | 7 | 0.66 (0.27, 1.61) | 0.36 | 34 | 1.25 (0.74, 2.10) | 0.40 | <10 | 1.29 (0.41, 4.08) | 0.66 |
| Prostate Cancer | ||||||||||||
| No | 55 | 1.0 (Ref) | 15 | 1.0 (Ref) | 57 | 1.0 (Ref) | 20 | 1.0 (Ref) | ||||
| Yes | 100 | 0.98 (0.70, 1.37) | 0.90 | <10 | 2.57 (0.81, 8.16) | 0.11 | 42 | 0.67 (0.44, 1.02) | 0.06 | <10 | 0.54 (0.13, 2.19) | 0.39 |
| Lung/Bronchus Cancer | ||||||||||||
| No | 161 | 1.0 (Ref) | 208 | 1.0 (Ref) | 100 | 1.0 (Ref) | 123 | 1.0 (Ref) | ||||
| Yes | 369 | 1.28 (1.06, 1.55) | 0.01 | 70 | 0.82 (0.61, 1.10) | 0.18 | 108 | 1.05 (0.79, 1.40) | 0.71 | 24 | 0.99 (0.62, 1.57) | 0.96 |
| Colorectal Cancer | ||||||||||||
| No | 66 | 1.0 (Ref) | 35 | 1.0 (Ref) | 57 | 1.0 (Ref) | 32 | 1.0 (Ref) | ||||
| Yes | 114 | 0.91 (0.66, 1.26) | 0.57 | 14 | 0.74 (0.36, 1.52) | 0.41 | 46 | 0.97 (0.63, 1.49) | 0.88 | <10 | 0.51 (0.18, 1.41) | 0.20 |
Breast cancer models were adjusted for enrollment source, years between study enrollment and cancer diagnosis, age, race, surgery, stage, smoking history, body mass index, COPD, mammogram, breast cancer subtype and menopausal status. Prostate cancer models were adjusted for: enrollment source, years between study enrollment and cancer diagnosis, race, age, surgery, stage, smoking history, body mass index, COPD, and prostate-specific antigen test. Lung cancer models were adjusted for: enrollment source, years between study enrollment and cancer diagnosis, race, age, sex, surgery, stage, smoking history, body mass index, COPD, and lung cancer subtype. Colorectal cancer models were adjusted for: enrollment source, years between study enrollment and cancer diagnosis, age, sex, race, surgery, stage, smoking history, body mass index, COPD, colonoscopy and tumor site, as appropriate.
Across other cancer types, Black individuals with an AHI less than $15,000 had a slightly higher hazard of death versus Whites for female breast cancers (Overall HR 1.20, 95%CI 0.85–1.70; Cancer-specific HR 1.27, 95%CI 0.79–2.04) and for colorectal cancers (Overall HR 1.10, 95%CI 0.78–1.56; Cancer-specific HR 1.08, 95%CI 0.69–1.67)—although these differences did not reach statistical significance (Table 2 and Supplementary Table 1). No racial differences in survival were observed for prostate cancers—potentially due to limited events in this cohort. We also repeated our primary analyses while excluding patients with an AHI of at least $50,000, and our results remained unchanged (Supplementary Table 3).
DISCUSSION
In this cohort study of low-income Black and White Americans diagnosed with breast, prostate, lung or colorectal cancer in the Southeastern United States, we found racial disparities in survival outcomes among individuals diagnosed with lung cancer who reported an AHI less than $15,000. Individuals with lung cancer who identified as Black had a 22% decreased hazard of death compared to Whites after accounting for individual-level and clinical characteristics, including smoking history, COPD, persistent poverty and lung cancer subtype.
Our discovery that Black individuals diagnosed with lung cancer who reported an AHI less than $15,000 have a reduced hazard of death compared with White counterparts is striking. This is because a robust body of literature has shown that overall Black patients with lung cancer have a poorer survival than White patients. Historically, individuals who identify as Black are less likely to be diagnosed early, less likely to receive any guideline-recommended treatment, including surgery, and have poorer survival outcomes compared with Whites.(13) However, studies to date have not been conducted including a sizable number of low-income individuals with an AHI less than $15,000. Within this population of low-income Americans, recent work exploring the impact of poverty on all-cause mortality revealed that poor White Americans experienced higher all-cause mortality than poor Black Americans.(14) Similar outcome patterns were observed across three neighborhood areas in Detroit (Rosedale Park, Pershing and Denby).(15) Together, these findings point to additional, translational research studies needed to better understand the relative contributions of residential environments and concentrated poverty on low-income populations and to disentangle complex biological and psychological adaptations that may uniquely drive carcinogenic processes.
Aligned with prior research, herein we observed that a lower proportion of Black individuals with an AHI less than $15,000 underwent surgical resection after lung cancer diagnosis versus White counterparts. However, among individuals with an AHI less than $15,000, we also observed racial differences by smoking history—as the population of Black individuals was comprised of a greater proportion of non-smokers compared to Whites. A potential explanation for our observation that individuals with an AHI less than $15,000 who identify as Black have a reduced hazard of death after lung cancer diagnosis may also be driven by tumor characteristics (e.g., histology, genetics, somatic variants)(16) and medical history (e.g., family history of lung cancer). This is supported by accumulating evidence that lung cancers arising in never smokers are a distinct entity from those arising in smokers.(17) While all histological types of lung cancer are associated with smoking, adenocarcinoma is the most common form of lung cancer in never smokers. Herein we observed that adenocarcinomas comprised a greater proportion of the lung cancers diagnosed among individuals who identify as Black in this population versus those identifying as White. Somatic mutation patterns and frequencies also differ between lung cancers in never smokers and smokers—particularly in TP53, KRAS and epidermal growth factor receptor (EGFR).(18–21) Non-smoking status is also a strong clinical predictor of benefit from EGFR tyrosine kinase inhibitors.(22) Although these genomic characteristics are currently unable to be assessed in our cohort, a deeper understanding of these tumor biological features together with environmental exposures within the population of individuals with an AHI less than $15,000 will be critical in future studies to disentangle the patterns we observed herein and to better understand the mechanisms of carcinogenesis as well as clinical outcomes in underserved populations with cancer. Additionally, while our observation that a lower proportion of Black individuals with an AHI less than $15,000 underwent surgical resection compared with Whites may be attributable to clinical disease presentation, it also draws attention to the importance of equity in access to high-quality cancer care services across low-income populations.
In contrast the observed lung cancer disparities by self-identified race among individuals with an AHI less than $15,000, Black females had a slightly higher hazard of death versus Whites for breast cancers, although the difference did not reach statistical significance. Moreover, we did not observe racial differences in outcomes among individuals in this cohort with colorectal or prostate cancers. This may be attributable to the overall fatality of lung cancer in this cohort, the limited number of events for specific malignancies (e.g., colorectum), and the differences in nation-wide screening rates across cancer types.(23) Notwithstanding this rationale, it is worthwhile to note that across all cancer types studied herein that outcomes did not differ by race for individuals with an AHI of at least $15,000 in the Southeastern United States. While deeper investigations are called upon to understand cancer-specific (e.g., colonoscopy screening, tumor mutational burden, nurse navigator access, therapeutic regimens, refusal for therapy) and individual-level factors (e.g., family cancer history, health literacy, occupation, access to transportation) that may be impacting these patterns, equivocal access to high-quality cancer care services, from prevention through treatment, harbors immense opportunity to improve clinical outcomes and move toward health equity across diverse, underserved populations.
We acknowledge the limitations of our study. First, we were unable to study cancer recurrence as the outcome as this information was not collected reliably in the SCCS. Second, we were unable to adjust AHI by family size, which inevitably influences the poverty threshold. For example, in 2009—the final year of SCCS recruitment, the United States Census Bureau set the AHI poverty threshold at $10,830 for a 1-person family.(24) A $3,740 increase was added to this base measure for each additional person in a family (e.g., $14,570 threshold for a 2-person family). Thus, individuals with an AHI less than $15,000 in the SCCS cohort would fall below the federal poverty line if there were less than 3 persons in their family. Third, AHI was assessed at baseline study enrollment; thus, we were unable to capture individuals’ AHI at the time of cancer diagnosis. As persistent poverty distinctly contributes to cancer mortality,(3) we acknowledge the limitations of using census-tract data for this measure and call for future comprehensive investigations into longitudinal-based poverty measures, unexpected negative events (e.g., housing instability, food insecurity) and additional social determinants of health with overall cancer burden—particularly across the Southeastern United States. Moreover, given that four out of every five individuals with an AHI of at least $15,000 in this cohort also reported an AHI less than $50,000, we also acknowledge our limited ability to observe patterns between low-income and high-income populations diagnosed with cancer. Lastly, with SCCS enrollment restricted to individuals aged 45 years and older, most cancers in this cohort were diagnosed after the age of 50. Given the rising tide of cancers diagnosed among individuals younger than age 50,(25) there stands a timely need to disentangle factors that are underpinning a distinct cancer burden in younger generations in future studies. Additionally, with the accumulation of recent data to support that molecular tumor features differ across population groups,(26–28) it is crucial to acknowledge that we were largely unable to elucidate how differences in genetics and tumor biology (e.g., germline and somatic variants) may impact disease-specific outcomes—which warrants further investigation.
Overall, this cohort study of low-income Americans who identified as Black and White in the Southeastern United States found that survival after lung cancer diagnosis significantly differed by race among individuals who reported an AHI less than $15,000. We observed that individuals who identified as Black had a significantly lower hazard of death compared with those who identified as White, even after adjusting for clinicodemographic and lifestyle factors. Further studies of the clinical, social, and structural characteristics of patients diagnosed with lung cancer in the Southeastern United States are needed in order to improve survival and access to high-quality cancer care services as well as mitigate cancer inequities.
Supplementary Material
ACKNOWLEDGEMENTS
We extend our gratitude to the individuals who have participated in the Southern Community Cohort Study (SCCS). This work was, in part, supported by Pfizer, Inc. The SCCS was supported by the National Cancer Institute of the National Institutes of Health under Award Number U01CA202979 (W. Zheng). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
A.N.H. is Chair of the Scientific Advisory Board for the Appendix Cancer Pseudomyxoma Peritonei (ACPMP) Research Foundation and reports receiving personal fees from MJH Life Sciences and Bayer AG outside the submitted work. FK was a Pfizer employee and shareholder. LJR and JPS are Pfizer employees and shareholders. Research reported in this publication was supported, in part, by National Institutes of Health under Award Number U01CA202979. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Footnotes
Disclosure of Potential Conflicts of Interest:
All other authors declare no conflicts of interest.
Data Availability
Data used in this project can be obtained directly from the SCCS by submitting a data request proposal (https://www.southerncommunitystudy.org/).
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
Data used in this project can be obtained directly from the SCCS by submitting a data request proposal (https://www.southerncommunitystudy.org/).