Amany R. Keruakous
Noha Soror
Sarah Jiménez
Rachel Ashley1- 1Department of Internal Medicine, Georgia Cancer Center, Augusta University at Medical College of Georgia, Augusta, GA, United States
- 2Section of Hematology-Oncology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, United States
- 3Mercer County Community College, West Windsor, NJ, United States
- 4Prisma Health, Columbia, SC, United States
Introduction
Cancer is one of the leading causes of death worldwide. It continues to be the second leading cause of death in the United States despite all national efforts aiming to reduce cancer burden and mortality. Per the Centers of Disease Control and Prevention (CDC), 602,350 deaths in the United States were attributed to cancer in 2019 (1). Improving cancer screening metrics is a crucial healthcare goal, with emerging data showing a significant reduction in compliance rate to cancer screening throughout the U.S., specifically amid overwhelmed healthcare system due to the current COVID-19 Pandemic (2). Cancer screening is an essential element of early cancer detection. Early diagnosis is a key determinant of timely treatment and survival outcomes for cancer patients and remains a cost-effective means of reducing cancer mortality. Delays in medical care and age-appropriate screening lead to increased cancer burden, reflecting the overall prognosis. In the United States of America, one-third of the adult population has cited challenges in medical care accessibility.
According to the current United States Preventive Task Force (USPSTF) recommendations, biennial screening mammography is recommended for women aged 45–74 years (3). For colorectal cancer screening, the USPSTF recommends screening in all adults aged 50–75 years (4, 5). The USPSTF recommends screening all females aged 21–29 every 3 years with cervical cytology alone for cervical cancer screening. For women aged 30–65 years, the USPSTF recommends screening every 3 years with cervical cytology alone, every 5 years with high-risk human papillomavirus (hrHPV) testing alone, or every 5 years with hrHPV testing in combination with cytology (co-testing) (6).
Adults aged 50–80 years who have a 20-pack-year smoking history and currently smoke or have quit within the past 15 years are recommended to be screened for lung cancer with low-dose computed tomography (LDCT). However, for prostate cancer screening for men aged 55–69, periodic prostate-specific antigen (PSA)-based screening for prostate cancer is recommended to be individualized (7).
Unfortunately, these cancer screening tools are not distributed equally across the U.S. population, with evidence of health care disparities in economically disadvantaged regions (8, 9).
Despite Medicaid expansion, which increased health insurance coverage and improved access to healthcare services for low-income Americans (10), racial and ethnic disparities are still problematic, with a wide gap in the healthcare system (11, 12).
Appropriate interventions to maximize screening in racial/ethnic minorities must be targeted toward the most vulnerable patient populations.
Aims
This Perspective aims to report the sociodemographic healthcare disparities and the challenges in medical services accessibility due to financial burden. Identifying the barriers to utilizing age-appropriate screening is key to delivering a more precise approach to overcoming healthcare disparities.
Methods
Using the Behavioral Risk Factor Surveillance System (BRFSS) questionnaire, we conducted a descriptive summary of 2020 BRFSS survey respondents. Data were analyzed to report the healthcare disparities of respondents to the 2020 BRFSS survey. We reviewed responses from participants who failed to have age-appropriate screening for breast and colon cancer.
Results
Factors identified to explain the advanced stage of cancer diagnosis and higher cancer mortality in underserved communities include lower socioeconomic status, lack of access to health care, lower rates of routine screening, and a lower likelihood of receiving recommended treatment for cancer (13).
We noticed from the BRFSS responses that among oncology patients, there was a higher proportion of unemployment, lower level of education, and lower annual income. However, the majority of them had health care coverage.
We report the impact of medical care's financial burden on cancer patients and its association with racial and socioeconomic disparities. We divided the patients based on their responses to the question, “Ever had difficulty seeing a physician due to medical cost?” and stratified the respondents based on racial and socioeconomic factors.
The proportion of participants who have difficulty seeing a physician due to cost varies between race and ethnicity. Multiracial minorities are approximately three times higher than the White race population to report the financial burden. In addition, the annual income, education level, and employment status are essential factors, with a higher financial burden among the lower annual income group (< 25k) and among participants who did not finish high school. African American participants had a higher percentage of lower annual income and higher unemployment rates.
We report compliance rates to age-appropriate screening and its association with socioeconomic status. There were differences between the groups of participants who delayed medical care due to cost vs. not; we reported lower compliance rates to screening mammography and colonoscopy for patients who reported financial difficulties accessing medical care.
The compliance with screening colonoscopy was affected by accessibility to medical care and medical cost; additionally, it was associated with the participants' race. For all cancer patients, participants of Asian, Hispanic, American Indian, and multiracial descent had higher non-compliance rates when compared to White or African-American descent. The non-compliance rates were even higher among the financially burdened population, across all races, with more pronounced differences in the Asian and Hispanic participants.
The responses for screening mammography are better, with lower rates of non-compliance across all races, compared to colon cancer screening. Moreover, there is still room for improvement among Hispanic and multiracial descent. The same observation is consistent for screening mammography, with higher rates of non-compliance among participants who reported delays in medical care due to cost.
We report that compliance with age-appropriate screening tools is lower among participants who had difficulties accessing medical care due to overbearing medical costs. We could determine that securing a healthcare coverage plan for the patients is critical to remediate compliance.
Discussion
There is a good body of evidence that improving health care coverage reflects on the screening rates and compliance (14–16).
Not only healthcare coverage but racial and socioeconomic disparities and level of education are crucial to delays in medical care. Future research and interventions should target those minorities to improve cancer care.
Medicaid expansion in certain states caused more significant improvement in total insurance and Medicaid coverage and mammogram rates in lower-income women than in non-expansion states after Medicaid legislation was passed. Studies demonstrated that people take advantage of expanded eligibility by acquiring insurance, which can improve access to preventive measures, such as screening mammography and colonoscopy (14, 15).
Adults with low income may lack insurance coverage through work but earn income just above the minimum amount needed to qualify for governmental low-income insurance programs, such as Medicaid (17, 18).
Unemployment is a significant factor evident among all racial classes in the U.S., which is more pronounced with the COVID-19 pandemic and our aging cancer population. COVID-19 pandemic has an adverse employment change and may have harmful impacts on workers' mental health, with disproportionate effects on racial minorities (19–21). The unemployed patient population is expanding, and efforts should be directed toward improving cancer care. There is a higher proportion of unemployment among the African American population.
Cultural perceptions are also barrier for age-appropriate cancer screening. The general attitude toward health care can be a challenge for appropriate cancer screening. Cultural perceptions can also affect patient decisions more than healthcare providers realize. For example, the diagnosis of “cancer” carries a stigma in many cultures (22). This can be related to associations and cultural believes that cancer is attributable to some form of bad luck or will of a supreme power. Therefore, it is crucial for healthcare providers to understand that such cultural perceptions of cancer can negatively impact screening rates and perception of importance of such preventive measures (23, 24).
Other religious values, and cultural practices that can hinder appropriate cancer screening can include, a false perception that the risk of cancer is low in certain ethnic groups, faith in traditional remedies, or viewing cancer as a sentence of death (25). Other specific cultural barriers to cancer screening for pelvic and breast malignancies is the cultural perception of modesty among women or concerns about preserving sexual function in men in certain cultural backgrounds (24). Lack of printed translated brochures/ patient education materials, lack of trust of the healthcare system and receiving less provider recommendation for cancer screening are more exacerbated by health care providers who fail to fully estimate and overcome those barriers (26, 27).
Cultural barriers might also make certain groups to be less information-seeking, and less accepting of screening for disease in the absence of symptoms compared to other groups (24).
Another factor that can affect recipients of appropriate screening is the out-of-pocket costs, even in population categories that are not considered low-income despite being insured. Dorn et al. examined colorectal cancer screening and observed that those with insurance reported significant declines in colonoscopy despite being insured in those with high out-of-pocket costs (28).
Other studies investigated racial disparities in breast cancer screening in A.A. women with findings of increased mammography rates. The authors postulated that the increasing mammography rates in this category might be due to a higher percentage of A.A. women having qualified for public insurance (29), which is another resource for racial minorities.
Other factors that potentiate racial inequalities include quality of housing, access to healthy food, transportation needs, and violence. Low awareness of screening guidelines, lack of appropriate access to information about the availability of new screening tools, cultural misbeliefs about screening, understanding of the risk, the stigmata of cancer, and the lack of access to facilities with cancer screening programs were all factors that negatively impacted colorectal screening (30). These factors altogether can widen the gap in access to health care (31).
Addressing these critical gaps in healthcare and screening tools access requires better data collection on racial inequalities in the healthcare system, increased research on racial and socioeconomic-sensitive policies, increased awareness of these disparities among healthcare professionals and leadership personnel in positions of implementing healthcare policies, and finally involving racial minorities in the development of these practice-changing policies.
Summary and recommendations
In summary, our Perspective summarizes health disparities and the barriers to compliance with screening tools. Due to the financial burden, delayed medical care is more pronounced in racial minorities, low socioeconomic status, and unemployed patients and should be targeted in future quality improvement projects. Given the harmful effects of delayed diagnosis and treatment of cancer, public health and clinical professionals must utilize tools to improve cancer screening accessibility to minorities with socioeconomic and racial disparities.
Author contributions
All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
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References
1. QuickStats: Age-Adjusted Death Rates* for Cancer by Urban-Rural Status(dagger) and Sex - National Vital Statistics System United States 1999-2019. MMWR Morb Mortal Wkly Rep. (2021) 70:1312. doi: 10.15585/mmwr.mm7037a8
2. Dennis LK, Hsu CH, Arrington AK. Reduction in standard cancer screening in 2020 throughout the U.S. Cancers. (2021) 13:5918. doi: 10.3390/cancers13235918
3. Farr DE, Brandt HM, Adams SA, Haynes VE, Gibson AS, Jackson DD, et al. Examining breast cancer screening behavior among southern black women after the 2009 US preventive services task force mammography guideline revisions. J Community Health. (2020) 45:20–9. doi: 10.1007/s10900-019-00697-8
4. Haghighat S, Sussman DA, Deshpande A. US preventive services task force recommendation statement on screening for colorectal cancer. JAMA. (2021) 326:1328. doi: 10.1001/jama.2021.13466
5. Wolf AMD, Fontham ETH, Church TR, Flowers CR, Guerra CE, LaMonte SJ, et al. Colorectal cancer screening for average-risk adults: 2018 guideline update from the American Cancer Society. CA Cancer J Clin. (2018) 68:250–81. doi: 10.3322/caac.21457
6. Fontham ETH, Wolf AMD, Church TR, Etzioni R, Flowers CR, Herzig A, et al. Cervical cancer screening for individuals at average risk: 2020 guideline update from the American Cancer Society. CA Cancer J Clin. (2020) 70:321–46. doi: 10.3322/caac.21628
7. Leapman MS, Wang R, Park H, Yu JB, Sprenkle PC, Cooperberg MR, et al. Changes in prostate-specific antigen testing relative to the revised US preventive services task force recommendation on prostate cancer screening. JAMA Oncol. (2022) 8:41–7. doi: 10.1001/jamaoncol.2021.5143
8. Braun KL, Stewart S, Baquet C, Berry-Bobovski L, Blumenthal D, Brandt HM, et al. The National Cancer Institute's community networks program initiative to reduce cancer health disparities: outcomes and lessons learned. Prog Community Health Partnersh. (2015) 9(Suppl):21–32. doi: 10.1353/cpr.2015.0017
9. DeSantis CE, Ma J, Goding Sauer A, Newman LA, Jemal A. Breast cancer statistics, 2017, racial disparity in mortality by state. CA Cancer J Clin. (2017) 67:439–48. doi: 10.3322/caac.21412
10. Sommers BD, Gunja MZ, Finegold K, Musco T. Changes in self-reported insurance coverage, access to care, and health under the affordable care act. JAMA. (2015) 314:366–74. doi: 10.1001/jama.2015.8421
11. May FP, Yang L, Corona E, Glenn BA, Bastani R. Disparities in colorectal cancer screening in the united states before and after implementation of the affordable care act. Clin Gastroenterol Hepatol. (2020) 18:1796. doi: 10.1016/j.cgh.2019.09.008
12. Eder M, Henninger M, Durbin S, Iacocca MO, Martin A, Gottlieb LM, et al. Screening and interventions for social risk factors: technical brief to support the US preventive services task force. JAMA. (2021) 326:1416–28. doi: 10.1001/jama.2021.12825
13. Donohoe J, Marshall V, Tan X, Camacho FT, Anderson RT, Balkrishnan R. Spatial access to primary care providers in appalachia: evaluating current methodology. J Prim Care Community Health. (2016) 7:149–58. doi: 10.1177/2150131916632554
14. Toyoda Y, Oh EJ, Premaratne ID, Chiuzan C, Rohde CH. Affordable care act state-specific medicaid expansion: impact on health insurance coverage and breast cancer screening rates. J Am Coll Surg. (2020). doi: 10.1016/j.jamcollsurg.2020.01.031
15. Carney PA, O'Malley J, Buckley DI, Mori M, Lieberman DA, Fagnan LJ, et al. Influence of health insurance coverage on breast, cervical, and colorectal cancer screening in rural primary care settings. Cancer. (2012) 118:6217–25. doi: 10.1002/cncr.27635
16. Garces-Palacio IC, Altarac M, Kirby R, McClure LA, Mulvihill B, Scarinci IC. Contribution of health care coverage in cervical cancer screening follow-up: findings from a cross-sectional study in Colombia. Int J Gynecol Cancer. (2010) 20:1232–9. doi: 10.1111/IGC.0b013e3181e8dfb8
17. Rosenbaum S, Wilensky G. Closing The medicaid coverage gap: options for reform. Health Aff. (2020) 39:514–8. doi: 10.1377/hlthaff.2019.01463
18. Dickinson H, Logie J, Mu G. Mind the gap: a comparison of encounter location and medical costs during the one-month periods immediately before and after a short gap in United States Medicaid healthcare coverage. Pharmacoepidem Dr S. (2019) 28:296–7.
19. Llop-Girones A, Vracar A, Llop-Girones G, Benach J, Angeli-Silva L, Jaimez L, et al. Employment and working conditions of nurses: where and how health inequalities have increased during the COVID-19 pandemic? Hum Resour Health. (2021) 19:112. doi: 10.1186/s12960-021-00651-7
20. Margolies PJ, Chiang IC, Jewell TC, Broadway-Wilson K, Gregory R, Scannevin G Jr, et al. Impact of the COVID-19 pandemic on a statewide individual placement and support employment initiative. Psychiatr Serv. (2021) appips202100120. doi: 10.1176/appi.ps.202100120
21. Gil D, Dominguez P, Undurraga EA, Valenzuela E. Employment loss in informal settlements during the Covid-19 pandemic: evidence from Chile. J Urban Health. (2021) 98:622–34. doi: 10.1007/s11524-021-00575-6
22. Phillips J. Unequal treatment: confronting racial and ethnic disparities in healthcare. Oncol Nurs Forum. (2004) 31:1019.
23. Ong KJ, Back MF, Lu JJ, Shakespeare TS, Wynne CJ. Cultural attitudes to cancer management in traditional South-East Asian patients. Australas Radiol. (2002) 46:370–4. doi: 10.1046/j.1440-1673.2002.t01-1-01085.x
24. Lee RJ, Madan RA, Kim J, Posadas EM, Yu EY. Disparities in cancer care and the asian american population. Oncologist. (2021) 26:453–60. doi: 10.1002/onco.13748
25. Facione NC, Giancarlo C, Chan L. Perceived risk and help-seeking behavior for breast cancer. A Chinese-American perspective. Cancer Nurs. (2000) 23:258–67. doi: 10.1097/00002820-200008000-00002
26. May FP, Almario CV, Ponce N, Spiegel BM. Racial minorities are more likely than whites to report lack of provider recommendation for colon cancer screening. Am J Gastroenterol. (2015) 110:1388–94. doi: 10.1038/ajg.2015.138
27. Glick SB, Clarke AR, Blanchard A, Whitaker AK. Cervical cancer screening, diagnosis and treatment interventions for racial and ethnic minorities: a systematic review. J Gen Intern Med. (2012) 27:1016–32. doi: 10.1007/s11606-012-2052-2
28. Dorn SD, Wei D, Farley JF, Shah ND, Shaheen NJ, Sandler RS, et al. Impact of the 2008-2009 economic recession on screening colonoscopy utilization among the insured. Clin Gastroenterol Hepatol. (2012) 10:278–84. doi: 10.1016/j.cgh.2011.11.020
29. King CJ, Chen J, Garza MA, Thomas SB. Breast and cervical screening by race/ethnicity: comparative analyses before and during the great recession. Am J Prev Med. (2014) 46:359–67. doi: 10.1016/S0749-3797(14)00089-0
30. Richman I, Asch SM, Bhattacharya J, Owens DK. Colorectal cancer screening in the era of the affordable care act. J Gen Intern Med. (2016) 31:315–20. doi: 10.1007/s11606-015-3504-2
Keywords: racial disparities, cancer care, cancer screening, racial minorities, socioeconomic status
Citation: Keruakous AR, Soror N, Jiménez S, Ashley R, Keruakous M and Sadek BT (2023) Barriers driving health care disparities in utilization of age-appropriate screening. Front. Public Health 11:1100466. doi: 10.3389/fpubh.2023.1100466
Received: 16 November 2022; Accepted: 15 February 2023;
Published: 03 March 2023.
Edited by:
Nera Agabiti, Regional Health Service of Lazio, ItalyReviewed by:
Amir Yosef, Mayo Clinic, United StatesCopyright © 2023 Keruakous, Soror, Jiménez, Ashley, Keruakous and Sadek. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Amany R. Keruakous, akeruakous@augusta.edu