Examining the Influence of Cost Concern and Awareness of Low-cost Health Care on Cancer Screening among the Medically Underserved

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Examining the Influence of Cost Concern and Awareness of Low-cost Health Care on Cancer Screening among the Medically Underserved Alicia L. Best, Alcha Strane, Omari Christie, Shalanda Bynum, Jaqueline Wiltshire Journal of Health Care for the Poor and Underserved, Volume 28, Number 1, February 2017, pp. 79-87 (Article) Published by Johns Hopkins University Press DOI: https://doi.org/10.1353/hpu.2017.0010 For additional information about this article https://muse.jhu.edu/article/648748 No institutional affiliation (11 Sep 2018 20:16 GMT)

BRIEF COMMUNICATION Examining the Influence of Cost Concern and Awareness of Low- cost Health Care on Cancer Screening among the Medically Underserved Alicia L. Best, PhD, MPH, CHES Alcha Strane, BS Omari Christie, BS, MS Shalanda Bynum, PhD, MPH Jaqueline Wiltshire, PhD, MPH Abstract: African Americans suffer a greater burden of mortality from breast, cervical, and colorectal cancers than other groups in the United States. Early detection through timely screening can improve survival outcomes; however, cost is frequently reported as a barrier to screening. Federally qualified health centers (FQHCs) provide preventive and primary care to underserved populations regardless of ability to pay, positioning them to improve cancer screening rates. The purpose of this study was to examine the influence of concern about health care cost (cost concern) and awareness of low- cost health care (awareness) on cancer screening among 236 African Americans within an FQHC service area using self- report surveys. Multiple logistic regression indicated that awareness was positively associated with cervical and colorectal cancer screening, while cost concern was negatively associated with mammography screening. Results indicate that improving awareness and understanding of low- cost health care could increase cancer screening among underserved African Americans. Key words: Cancer screening, medically underserved, cost concern, awareness, federally qualified health center. Breast, cervical, and colorectal cancers (CRC) are highly prioritized in the fight against cancer- related health disparities due to the life- saving benefits of screening. 1,2 Despite this increased priority, African Americans continue to bear disproportionately high burdens of these diseases. 3 African Americans are more likely than non- Hispanic Whites to die of breast, cervical, and CRC. 4 In spite of the promise of screening, many African Americans (especially low- income) underutilize cancer screening services and consequently are more likely to be diagnosed with later- stage disease compared with non-hispanic Whites. 5 ALICIA BEST is associated with The University of South Florida, College of Public Health, Department of Community and Family Health. ALCHA STRANE and OMARI CHRISTIE are associated with Morehouse School of Medicine. SHALANDA BYNUM is associated with National Institutes of Health, Center for Scientific Review. JAQUELINE WILTSHIRE is associated with The University of South Florida, Department of Health Policy and Management. Meharry Medical College Journal of Health Care for the Poor and Underserved 28 (2017): 79 87.

80 Cost concern, awareness, and cancer screening Individuals with low socioeconomic status (SES) are more likely than those with higher SES to report cost as the primary barrier to receiving health care. 6 Low SES is highly correlated with cancer risks and negative outcomes due to lack of or inadequate health insurance, reduced access to recommended preventive care and treatment services, and low literacy levels. 6 These factors disproportionately affect African Americans, as African Americans are more likely than non- Hispanic Whites to be uninsured and live below the federal poverty threshold. 5 A medically underserved population (MUP) is described as having limited primary care providers, above average infant mortality, high rates of poverty, and/or high elderly population. 7 To improve access to health care among MUPs, the Federally Qualified Health Center (FQHC) benefit was introduced under the Medicare Act, 8 and expanded with the 2010 passage of the Affordable Care Act. 9 These health centers can be invaluable partners in reducing cancer- related health disparities due to their mission of providing services regardless of ability to pay, and their strategic location in medically underserved areas. 10 Offering care on income- based sliding- fee scales, FQHCs are required to accept all patients even if they cannot pay for services. However, FQHCs are underutilized in many communities, and underserved populations still present to hospital emergency departments for primary care or in tertiary stages of disease. 11 This could be due, in part, to lack of awareness and/or understanding of the FQHC s role in alleviating cost concern among uninsured populations. Almufleh and colleagues found that after being referred to an FQHC for follow- up care for health screening results, individuals still cited lack of insurance and inability to afford services as the main reason for not adhering to follow- up recommendations. 12 This highlights the need for targeted research to help elucidate awareness and understanding of FQHCs among underserved populations, which would inform educational interventions. This study is one of few to examine awareness of low- cost health care among African Americans within an FQHC service area, while also examining the extent to which awareness of low- cost health care is associated with cancer screening. Specifically, this study aimed 1) to identify the extent to which adults accessing community resources within two miles of an FQHC were aware of low- cost health care in their area; and 2) to examine the extent to which awareness of low- cost health care and concern about health care cost were associated with cancer screening among a medically underserved population. We hypothesized that general awareness of low- cost health care resources such as FQHCs would be low. Further, we hypothesized that cost concerns would negatively influence cancer screening, while awareness of low- cost health care would positively influence screening. Methods Research design. Data were collected between August 2014 and March 2015 using self- reported surveys within a two- mile radius of an FQHC in Atlanta, Georgia. The assumption was that individuals accessing community resources within our target community (e.g., attending church, grocery shopping) should also be aware of and/ or use nearby health services. Potential participants were approached at various

Best, Strane, Christie, Bynum, and Wiltshire 81 community- based locations (e.g., a train station, libraries, churches, recreation centers, and grocery stores) and asked if they were interested in taking part in a study about health care. Participants were asked to read (or have read to them) and sign a consent form before completing a survey. Upon consent, participants completed a self- report survey using tablet- style personal computers (i.e., ipads) or paper- and- pencil format, depending on their preference. The surveys took approximately 12 minutes to complete and individuals were provided a small gift bag. This study was approved by the Institutional Review Board at the Morehouse School of Medicine. Participants and setting. A total of 236 African Americans completed surveys. Eligible participants included men and women who 1) were age 18 years and older; 2) self- reported as African American; 3) accessed at least one community resource within two miles of a particular FQHC in Metropolitan Atlanta during the study period; and 4) were able to speak and understand English. Measures. The survey instrument captured demographic and health- related variables. Demographic variables included age, gender, education level, and household income. Health- related variables included health insurance status, cancer screening, awareness of low- cost health care, and concern about health care cost. Awareness and cost concern. Primary independent variables included awareness of free and low- cost health care services (i.e., awareness) and concern about health care cost (i.e., cost concern). Awareness was assessed using a single item, Are you aware of free or low- cost health service providers in your area? Responses were coded as yes or no. Cost concern was created from an item that asked participants, Please indicate to what extent the following factors are barriers for you receiving health care. One sub- item was Cost of receiving medical care and participants rated the extent to which cost was a barrier on a five- point Likert scale ranging from Not a barrier at all to Always a barrier. We created a dichotomous indicator variable reflecting those who selected Not a barrier at all versus those who indicted that cost was ever a barrier to health care utilization. Cancer screening. The U.S. Preventive Services Task Force (USPSTF) recommends a screening mammography for breast cancer every other year for women aged 50 74, 13 and a Papanicolaou (Pap) test for cervical cancer screening every three years for women aged 21 65, or every five years in combination with human papillomavirus (HPV) testing for women 30 65. 14 At the time of survey administration, the five- year interval option had been out for less than two years. Therefore, women who were screened under the new guideline are captured in our up- to- date category, having been screening within three years. The USPSTF recommends screening for CRC using either annual fecal occult blood testing (FOBT), flexible sigmoidoscopy every five years, or colonoscopy every 10 years in adults aged 50 75. 15 Primary dependent variables included the following cancer screenings: 1) Pap test in the last three years (females, aged 21 65); 2) mammography screening in the last two years (females, aged 50 74); and 3) CRC screening ever (males and females, aged 50 75). These outcomes were assessed using the following items: A Pap Exam is a test for cancer of the cervix. When was your last Pap Exam? A mammogram is an x- ray of the breast to screen for breast cancer. When was your last mammogram? and [Colonoscopy, sigmoidoscopy, and blood stool test were described, followed by

82 Cost concern, awareness, and cancer screening the question] Have you had any of these tests to check for colon cancer? Response options for the Pap testing were dichotomized to indicate whether respondents were up- to- date (up to three years ago) or not up- to- date (more than three years ago or never had). Response options for the mammography item were also dichotomized to indicate whether respondents were up- to- date (up to two years ago) or not up- to- date (more than two years ago or never had). Response options for CRC screening item were yes and no. Data analysis. Descriptive statistics including frequencies, means, and standard deviations were calculated to describe demographic characteristics of the sample. Prior to conducting multivariate analyses, correlation analyses were conducted to avoid potential multicollinearity issues. Multiple logistic regression analyses were conducted to examine the influence of awareness and cost concern on cancer screening, adjusting for covariates. The survey item measuring participant income included a response option for Prefer not to answer. Approximately 19% of participants choose not to report their income; thus, regression models were not adjusted for income. Each regression model was run using the appropriate sub- sample based on USPSTF guidelines. 13 15 For all analyses, statistical significance was set to p <.05. All statistical analyses were conducted using SPSS version 22. 16 Results Sample description. Demographic characteristics of the sample are reported in Table 1. Approximately 65% of sample participants were female, and the average age was 46.8 years (SD = 15.3). Over 50% of participants reported having a high school diploma or less. More than a quarter of sample participants (26.7%) reported a household income of less than or equal to $10,000 per year, and nearly 30% indicated that they had no health insurance coverage. Awareness, cost concern, and cancer screening. Table 2 presents the results from univariate analyses describing awareness, cost concern, and cancer screening. Over 66% of study participants indicated that they were not aware of free or low- cost health care services in their area, and 56.4% reported that cost was a barrier to receiving health care. Of Pap- eligible participants, 67.4% reported having a Pap test in the last three years. Among mammography- eligible participants, 60% indicated that they had received a mammogram in the last two years. Among CRC screening- eligible participants, 45.4% reported ever having a CRC screening test. Multiple logistic regression. Results from logistic regression analyses are reported in Table 3. All regression models were adjusted for age, education level, and insurance status. Additionally, the model predicting CRC screening was adjusted for gender. Among Pap- eligible participants, those who were aware of low- cost health care were 6.46 times more likely to have had Pap test within the last three years (aor = 6.46, 95% CI: 2.21 18.88) compared with those who were not aware. Cost concern was not significantly associated with Pap screening. Among mammography- eligible participants, cost concern had a significant negative association with having a mammogram in the past two years (aor = 0.16, 95% CI: 0.05 0.55). Awareness was not significantly associated with mammography screening. Among CRC screening- eligible participants,

Best, Strane, Christie, Bynum, and Wiltshire 83 Table 1. DEMOGRAPHIC CHARACTERISTICS (N = 236) a Characteristic M(SD) n(%) Age (years) 46.8 (15.3) Gender Female 153 (64.8) Male 83 (35.2) Education Less than HS 19 (8.1) HS diploma/ged 100 (42.4) Some college 69 (29.2) College degree or more 46 (19.5) Income (US dollars) 10,000 63 (26.7) 10,001 25,000 52 (22.0) 25,001 40,000 42 (17.8) >40,000 32 (13.1) Prefer not to answer 44 (18.6) Insurance coverage Yes 166 (70.3) No 69 (29.2) a Missing data are not included; percentages may not total 100. those who were aware of low- cost health care were 4.63 times more likely to have ever had a CRC screening test (aor = 4.63, 95% CI: 1.58 13.55). Cost concern was not significantly associated with CRC screening. Discussion This study examined associations between cost concern, awareness of low- cost health care, and cancer screening among a medically underserved population. Findings indicate that, even after adjusting for health insurance status and other important socio- demographic characteristics, cost concern and awareness of low- cost health care are important predictors of cancer screening. It is also important to note that cost concern and awareness did not consistently predict screening across cancer sites. Specifically, awareness was positively associated with cervical and CRC screening, while cost concern was negatively associated with mammography screening. Awareness predicted cervical and CRC screening, but not mammography. One reason that cervical and CRC screening may be influenced by awareness is that Pap tests and certain CRC screening exams (e.g., FOBTs) are more assessable in underserved communities compared with mammograms. 17 18 Specifically, Paps and FOBTs are routinely offered at most community health centers and FQHCs. 17 19 Unlike mam-

84 Cost concern, awareness, and cancer screening Table 2. AWARENESS, COST CONCERN, AND CANCER SCREENING (N = 236) a Characteristic n(%) Awareness Yes 79 (33.5) No 156 (66.1) Cost concern Yes 133 (56.4) No 103 (43.6) Pap screening (n = 129) b Yes 87 (67.4) No 42 (32.6) Mammography screening (n = 70) c Yes 42 (60.0) No 28 (40.0) CRC screening (n = 107) d Yes 49 (45.4) No 59 (54.6) a Missing data are not included; thus percentages may not total 100. b Papanicolaou test in the last 3 years, women age 21 65 years. c Mammogram in the last 2 years, women age 50 74 years. d Fecal occult blood test, sigmoidoscopy, or colonoscopy ever, adults age 50 75 years. mography, patients may be more likely to adhere to a physician s recommendation for a Pap test or the initiation of a FOBT because patients are not usually referred out to other facilities for these screenings. Thus, being aware of a local FQHC or other community health center could increase cervical and CRC screening adherence among low- income populations. In the case of mammography, perceived cost continues to pose a barrier to screening adherence. Many FQHCs do not offer mammograms, so patients are referred out for screening. 20 Referral to another facility may amplify cost concern, while also introducing other barriers such as transportation and time constraints. To improve screening participation among populations that have difficulties accessing health services, it is critical to provide comprehensive services in the communities where these individuals live. Findings from the present study demonstrate that the mere presence of FQHCs in medically underserved areas may not fully address access to health care. In fact, over 66% of participants indicated that they were not aware of low- cost health services in their area. Additionally, cancer screening rates of study participants were lower than rates of the general population in the state. Specifically, Pap adherence rates are approximately 73%, and mammography adherence rates are approximately 81% in Georgia, 21 while Pap and mammography screening adherence rates in the current sample were

Best, Strane, Christie, Bynum, and Wiltshire 85 Table 3. LOGISTIC REGRESSION PREDICTING CANCER SCREENING p-value aor (95% CI) a Pap screening (n = 129) b Awareness of healthcare services <0.01 6.46 (2.21 18.88) Cost concern 0.07 0.45 (0.19 1.08) Mammography screening (n = 70) c Awareness of healthcare services 0.07 3.41 (0.91 12.73) Cost concern <0.01 0.16 (0.05 0.55) CRC screening (n = 107) d,e Awareness of healthcare services <0.01 4.63 (1.58 13.55) Cost concern 0.11 0.46 (0.18 1.19) a Adjusted for age, education, income and insurance status. b Pap screening in the last 3 years, women ages 21 65 years. c Mammography in the last 2 years, women ages 50 74 years. d Colon cancer test ever, men and women age 50 75 years. e Also adjusted for gender. 67.4% and 60%, respectively. Access to care is a multidimensional construct involving factors that facilitate or impede the opportunity to use health services. 22[p. 1196] Thiede and McIntyre posit that a critical dimension of health care access is information. 22 A concerted effort is needed to increase awareness of available resources among medically underserved populations. For example, FQHCs offer health care on a sliding- fee scale based on an individual s income, 10 which theoretically reduces cost as a barrier to accessing health care. However, previous research found that even after being referred to an FQHC, individuals still cited cost as a barrier to health care utilization. 12 Thus, targeted communication interventions are necessary to adequately explain the payment structure of FQHCs (i.e., sliding- fee scale), describe services offered through FQHCs and their affiliates, and increase overall awareness of the presence of FQHCs within medically underserved areas. Findings from this research should be interpreted in light of certain limitations. One such limitation is lack of specificity in assessing awareness of low- cost health care. Participants were not specifically queried about awareness of FQHCs, but more broadly about awareness of low- cost health care providers in their area. Additionally, the term low- cost may have different meanings for different participants. Because participants were asked if they ever had any CRC screening test, analyses could not be stratified by the different CRC screening modalities. Furthermore, self- report screening information was not cross- checked with medical record data; thus, there is potential for recall bias. Data were cross- sectional, which prohibits causal inferences. The sample size was small, particularly for individuals eligible for mammography screenings, which may have precluded detection of significant effects. Despite these limitations, this study is unique in that it is among the first to examine awareness of low- cost health care among

86 Cost concern, awareness, and cancer screening individuals within close proximity of an FQHC, and to examine how awareness and cost concern influence screening utilization. Conclusion. This study offers insights into two important dimensions of health care access awareness and cost among underserved populations. Results indicate that improving awareness and understanding of health care resources could increase cancer screening adherence among underserved African Americans. Federally qualified health centers can be invaluable partners in reducing cancer- related health disparities due to their mission of providing services regardless of ability to pay. Legislation such as the Affordable Care Act offers a promising solution to increasing access to health care for all. However, these programs will be minimally effective in reducing health disparities without raising awareness and understanding of these resources among the most vulnerable populations. Disclaimer The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health, Department of Health and Human Services, or the United States government. References 1. Plescia M, Richardson LC, Joseph D. New roles for public health in cancer screening. CA Cancer J Clin. 2012 Jul- Aug;62(4):217 9. Epub 2012 May 9. https://doi.org/10.3322/caac.21147 2. Hewitt M, Simone J. Institute of Medicine report: ensuring quality cancer care. Washington, DC: National Academy Press, 1999. 3. American Cancer Society. Cancer facts & Figures 2015. Atlanta, GA: American Cancer Society, 2015. 4. American Cancer Society. Cancer Facts & Figures for African Americans 2013 2014. Atlanta, GA: American Cancer Society, 2013. 5. National Cancer Institute. Cancer Health Disparities Fact Sheet. Bethesda MD: National Cancer Institute, 2008. Available at: http://www.cancer.gov/about- nci/organization /crchd/cancer-health-disparities-fact-sheet. 6. Fitzgerald N. Acculturation, socioeconomic status, and health among Hispanics. Napa Bulletin. 2010;34(1):28 46. https://doi.org/10.1111/j.1556-4797.2010.01050.x 7. Health Resources and Services Administration. Medically underserved areas/ populations: guidelines for MUA and MUP designation. Rockville, MD: Health Resources and Services Administration, 1995. Available at: http://www.hrsa.gov /shortage/mua/. 8. Centers for Medicare and Medicaid Services. Federally qualified health center fact sheet. Washington, DC: Centers for Medicare and Medicaid Services, 2009. Available at: file:///c:/users/abest/downloads/09aprilfqhcfactsheet.pdf. 9. Koh HK, Graham G, Glied SA. Reducing racial and ethnic disparities: the action plan from the department of health and human services. Health Aff (Millwood). 2011;30(10):1822 9. https://doi.org/10.1377/hlthaff.2011.0673

Best, Strane, Christie, Bynum, and Wiltshire 87 10. Health Resources and Services Administration. What are Federally Qualified Health Centers (FQHCs)? Washington, DC: Health Resources and Services Administration, 2007. Available at: http://www.hrsa.gov/healthit/toolbox/ruralhealthittoolbox /Introduction/qualified.html. 11. Agarwal P. Exploring Health Insurance Status and Emergency Department Utilization. Health Services Research and Managerial Epidemiology. Oct 2015;2:2333392815606094. https://doi.org/10.1177/2333392815606094 12. Almufleh A. Role of community health outreach program living for health in improving access to federally qualified health centers in Miami- dade county, Florida: a cross- sectional study. BMC Health Serv Res. 2015 Apr 28;15:181. https://doi.org/10.1186/s12913-015-0826-z 13. US Preventive Services Task Force. Screening for Breast Cancer: U.S. Preventive Services Task Force Recommendation Statement. Annals Intern Med. 2009 Feb 16;164(4):279 96. Epub 2016 Jan 12. 14. U.S. Preventive Services Task Force. Cervical Cancer: Screening. Rockville, MD: U.S. Preventive Services Task Force, 2012. Available at: 15. US Preventive Services Task Force. Screening for colorectal cancer: recommendation and rationale. Ann Intern Med. 2002 Jul 16;137(2):129 31. https://doi.org/10.7326/0003-4819-137-2-200207160-00014 16. IBM Corporation. IBM SPSS Statistics for Windows, Version 22.0. Armonk, NY: IBM Corporation, 2013. 17. Wolf MS. Colorectal cancer screening among the medically underserved. J Health Care Poor Underserved. 2006;17(1):47 54. https://doi.org/10.1353/hpu.2006.0037 18. Miller C, Takach M. A medical home framework for increasing cervical cancer screening rates: best practices for FQHCs. Washington, DC: National Academy for State Health Policy, 2013. Available at: http://www.nashp.org/sites/default/files/cerv _cancer.pdf. 19. Khankari K. Improving colorectal cancer screening among the medically underserved: a pilot study within a federally qualified health center. J Gen Intern Med. 2007 Oct;22(10):1410 4. Epub 2007 Jul 26. https://doi.org/10.1007/s11606-007-0295-0 20. Adams SA. Is Availability of Mammography Services at Federally Qualified Health Centers Associated with Breast Cancer Mortality- to- Incidence Ratios? An Ecological Analysis. J Womens Health (Larchmt). 2015 Nov;24(11):916 23. Epub 2015 Jul 24. https://doi.org/10.1089/jwh.2014.5114 21. Georgia Department of Public Health. Behavioral Risk Factor Surveillance System (BRFSS). Atlanta, GA: Georgia Department of Public Health, 2014. 22. Thiede M, McIntyre D. Information, communication and equitable access to health care: a conceptual note. Cad Saude Publica. 2008 May;24(5):1168 73. https://doi.org/10.1590/s0102-311x2008000500025