Abstract
Introduction
Breast cancer is the most common cancer (123.9 per 100,000 American women) and second deadliest cancer (20.5 per 100,000 American women) in 2014 (U.S. Cancer Statistics Working Group, 2015). Of newly diagnosed breast cancer cases each year, 40% occur in women over the age of 65 years, with 99,860 new breast cancer cases in this age group in 2013 (American Cancer Society, 2013; Howlader et al., 2016). Breast cancer relapse and mortality rates are higher in those 65 years and over than those aged 50 to 64 years (Howlader et al., 2016; van de Water et al., 2012). Fifty-eight percent of breast cancer–related deaths in 2015 occurred among women aged 65 years and over (American Cancer Society, 2015). Clinicians utilize mammograms for early detection of breast cancer. In 2012, clinicians either ordered or provided a mammogram at approximately 12.1 million physician visits (Centers for Disease Control and Prevention, 2016). However, changes in screening mammogram guidelines can contribute to changes in utilization (Lang, Nergarden, Andersson, Rosso, & Zackrisson, 2016; U.S. Preventive Services Task Force [USPSTF], 2009).
Prior to 2009, the USPSTF provided a “B” recommendation to screening mammograms for women aged 40 years and older every 1 to 2 years, stating that screening mammograms offered a moderate benefit (USPSTF, 2002). In November 2009, the updated USPSTF guideline recommended biennial screening mammograms for women aged 50 to 74 years (USPSTF, 2009). Also, as of November 2009, the USPSTF no longer recommended mammograms in women over age 74 years because the balance between benefits and harms for women in this age group was unclear.
Though screening mammograms are available to women aged 75 years and over, barriers to screening mammograms prevent women in this age group from undergoing this procedure. These women may be restricted from receiving a screening mammogram due to either disabilities or other comorbidities. However, the clinician may advise a screening if he or she thinks the procedure is necessary and the subject is in good health (Martin, 2015; Pace & Keating, 2014). Some studies have shown that physicians still have not implemented the revised 2009 USPSTF guidelines and prefer to assign mammograms on a case-by-case basis in women aged 75 years and over (Centers for Medicaid and Medicare Services, 2015; Corbelli et al., 2014; Hinz, Kudesia, Rolston, Caputo, & Worley, 2011; Kadivar et al., 2014).
In addition to changes in screening recommendations, changes in policy, such as the 2011 Affordable Care Act (ACA) implementation, may also affect screening mammogram utilization. The ACA increased access to preventive services, including screening mammograms for women aged 50-74 years (Mehta et al., 2015). Though stakeholders initially believed that the ACA would increase access to screening mammograms in all age groups, a recent study found that the policy application did not have an effect on screening among women in a younger population (age 50-64 years; Mehta et al., 2015). Given the higher incidence of breast cancer in older women (Howlader et al., 2014; Howlader et al., 2016; Mehta et al., 2015; van de Water et al., 2012), it is important to determine mammogram frequency before and after the 2011 ACA implementation to understand the policy impact of access to preventive services among women at the greatest risk of breast cancer.
This study examines screening mammograms in women aged 65 to 74 years and 75 and over years before and after the 2009 USPSTF recommendation changes and the 2011 ACA implementation. This study utilizes the Medicare Fee-For-Service (FFS) physician claims data in addition to the Medicare Current Beneficiary Survey (MCBS) from 2001 to 2013 to address changes in screening mammogram utilization in women aged 65 years and over. The relationship between the screening mammogram utilization in women 65 years and over and the USPSTF recommendation changes, despite the ACA increased access to screenings, remains unknown.
We hypothesize that among women aged 65 to 74 years, the utilization of annual screening mammograms will increase after the 2009 USPSTF recommendation changes and the 2011 ACA implementation. We also hypothesize that among women aged 75 years and over, for whom USPSTF has insufficient information to determine the net benefit of screening mammograms, the annual utilization of screening mammograms will gradually decrease after the 2009 USPSTF recommendation. We expect a decrease in the utilization of screening mammograms among women aged 75 years and over through the 2011 ACA implementation and beyond.
Method
Study Design
We used a repeated cross-sectional study design to examine trends in screening mammograms before and after the implementation of the USPSTF recommendations and the ACA implementation (Figure 1). We utilized sociodemographic data from the annual “access to care” files of the MCBS from 2001 to 2013. MCBS is an annual panel survey that can be administered up to 4 years per respondent. We examined physician claims data for annual screening mammogram claims to detect screening mammogram claims from 2001 to 2013. The sample included community-dwelling women aged 65 years and over in MCBS who did not have a history of breast cancer or mastectomy, according to self-report and claims data. The study received approval from the local institutional review board.

Timeline from 2001 to 2013.
Dependent Variable, Independent Variable, and Covariates
The dependent variable was receipt of an annual screening mammogram based on the screening mammogram Healthcare Common Procedural Coding System (HCPCS) codes in physician claims (Table 1) (Centers for Medicaid and Medicare Services, 2006; Jiang, Hughes, & Duszak, 2015). The independent variable was the year of the screening mammogram claim (2001-2013) with 2001 as the reference year.
Healthcare Common Procedural Coding System Codes Used in Analysis.
The analysis included the following covariates: census region, dual Medicare/Medicaid eligibility, educational level, income, and race/ethnicity. We categorized census region into east coast (New England, mid-Atlantic, south Atlantic, and Puerto Rico; reference), Central (east north central, west north central, east south central, and west south central), and west coast (Mountain and Pacific). Dual insurance eligibility status assessed whether women qualified for both Medicare and Medicaid at baseline. We stratified educational level into no high school diploma, high school diploma and/or vocational training, and higher than high school diploma (reference). We evaluated income as a dichotomous variable at either above US$25,000 (reference) or US$25,000 and below (Harrold et al., 2013). We categorized race/ethnicity as White (reference), African American, and Other.
Statistical Analysis
We described the distribution of sociodemographic characteristics of women receiving screening mammograms before (2001-2010) and after the ACA (2011-2013). To identify baseline characteristics for those with screening mammograms, we utilized up to 4 years of data per individual to determine whether she received a screening mammogram. We selected the most recent year an individual had a screening mammogram claim for descriptive analysis, if she ever had a screening mammogram, and classified the time-period based on the year with the most recent screening mammogram. To identify baseline characteristics among women who did not have a screening mammogram claim, we used the most recent year available. We used cross-sectional full sample weights from each year to calculate the mean sample weight for the pre-ACA and post-ACA periods (Table 2).
Demographics Characteristics of Women by Presence of Any Screening Mammogram by Time Period. a
Note. ACA = Affordable Care Act.
The most recent screening mammogram was used for each time-period.
p value < .0001 among those in the pre-ACA period and among those in the post-ACA period.
Weighted results reflect the general Medicare population.
We assessed the annual prevalence of screening mammogram by age. Covariate-adjusted and unadjusted logistic regression with generalized estimating equation (GEE) correction assessed the effect of the ACA implementation on screening mammogram utilization. Adjusted models controlled for race/ethnicity, geographic location, educational level, income level, and dual Medicare/Medicaid insurance status. We stratified the sample into age groups 65 to 74 years and 75 years and over due to the 2009 USPSTF recommendations. The GEE model in each age group accounted for repeated measures of annual screening mammograms across time. The exchangeable working correlation structure modeled after the compound symmetry covariance matrix was used. We performed statistical analyses using SAS Version 9.3 (Cary, NC).
Sensitivity Analyses
According to the survey data, patients with mammograms in the past year answered “yes” to the self-reported question:
Had you received a mammogram/breast X-ray in the past year?
Sensitivity analysis evaluated the positive predictive value (PPV) between women who answered yes to the self-reported mammogram question and had a screening mammogram claim in the same year. PPV is calculated by
where false positives are those who answered “yes” to the self-reported question but had no screening mammogram claim in that year. True positives are those who answered “yes” to the self-reported question and had a screening mammogram claim in that year. We used PPV to assess the ability of the self-reported questionnaire to predict a screening mammogram. PPV was calculated from 2001 to 2012 because the self-reported question changed in 2013 to “Had you received a mammogram/breast X-ray in the past 4 years?” which was no longer applicable to our study question.
Results
Pre-ACA, 26% (n = 18,791) of respondents had at least one screening mammogram during the 4-year MCBS study period, whereas 24% (n = 4,572) had one screening mammogram post-ACA. Table 2 depicts the weighted demographic characteristics of women undergoing screening mammograms from 2001 to 2013. Of those who had a screening mammogram pre-ACA, 55.9% were aged 65 to 74 years compared with 44% of those who did not have screening mammogram pre-ACA. Similarly, of those who had a screening mammogram post-ACA, 58.9% were aged 65 to 74 years compared with 46.9% of those who did not have screening mammogram post-ACA. Of those who did had a screening mammogram pre-ACA, 47.9% had an income of less than US$25,000 per year compared with 64.8% of those who did not have a screening mammogram pre-ACA. However, of those who had a screening mammogram post-ACA, 33.7% had an income of less than US$25,000 per year compared with 51.8% of those who did not have a screening mammogram post-ACA. Of those who had a screening mammogram pre-ACA, 18.6% had less than a high school diploma compared with 31.2% of those who did not have a screening mammogram pre-ACA. Post-ACA, 15.2% of those with screening mammogram had less than a high school diploma compared with 23.4% of those who did not have a screening mammogram.
In both age groups, the proportions of annual screening mammograms increased from 2001 to 2007 (Figure 2). The proportions of annual screening mammograms in women age 65 to 74 years started to decline after 2007, with the lowest frequency in 2011 of 27.6%. In the 75 years and over age group, prevalence of screening mammograms started to decline after 2011, with the lowest frequency in 2013 of 17.7%. Each year, the proportion of screening mammograms in those aged 65 to 74 years was higher than the older age group.

Annual proportions of screening mammograms among MCBS respondents by age group, 2001-2013.a
The adjusted odds of annual screening mammograms in women aged 65 to 74 were 25% lower in 2013 (odds ratio: 0.747; 95% confidence interval [CI]: 0.669-0.834) than the odds of screening mammograms pre-ACA (Table 3; reference year: 2001). The adjusted odds of screening mammograms in women aged 75 years and over were 33% lower in 2013 (odds ratio: 0.67; 95% CI: 0.602-0.745) than the odds of screening mammograms pre-ACA (reference year: 2001) as exhibited in Table 4.
Odds Ratios of Annual Screening Mammograms From 2001 to 2013 Among Women Aged 65 to 74 Years.
Odds ratios are adjusted for race/ethnicity, geographic location, educational level, income level, and dual Medicare/Medicaid insurance status.
Odds Ratios of Annual Screening Mammograms From 2001 to 2013 Among Women Aged 75+ Years.
Odds ratios are adjusted for race/ethnicity, geographic location, educational level, income level, and dual Medicare/Medicaid insurance status.
Table 5 assessed the ability of self-reported mammograms to predict screening mammogram utilization. Among women aged 65 to 74 years, PPV ranged from 43.1% to 53.5% from 2001 to 2012. Similarly, among those aged 75 years and over, PPV ranged from 44.9% to 50.5% during that time-period. The sensitivity analysis demonstrated that self-reported mammograms based on the survey question did not identify a large amount of screening mammogram utilization in those aged 65 to 74 years and 75 years and over (mean PPV: 0.485 and 0.473, respectively).
PPV of Self-Reported Mammograms for Identifying Subjects With Screening Mammograms by Age Group, 2001-2012.
Note. PPV = positive predictive value.
Discussion
The USPSTF update to recommendations in 2009 and the ACA implementation in 2011 were associated with decreases in screening mammogram utilization. In our study, screening mammogram proportions were higher in those aged 65 to 74 years at all time-points compared with those aged 75 years and over, for whom USPSTF cannot determine a recommendation of screening mammograms. These findings were consistent with a previous study from 2001 to 2007 (Salloum, Jensen, & Biddle, 2013). However, contrary to our hypothesis, screening mammogram proportions decreased after 2007 and did not increase following the ACA implementation. Though the adjusted odds of screening mammograms were expected to decrease in women aged 75 years and over due to the 2009 USPSTF recommendation changes, it was not expected in those aged 65 to 74 years. We previously hypothesized that the adjusted odds of screening mammograms in those aged 65 to 74 years would increase due to the ACA’s widespread access of this recommended, preventive service. Previous studies did not find an increase in screening mammogram utilization after the ACA implementation. One study found no effect of the ACA on screening mammograms among women aged 50 to 64 years, whereas another found no association among women 75+ years (Mehta et al., 2015; Nelson, Weerasinghe, Wang, & Grunkemeier, 2015).
Some studies, however, have reported different findings than our analysis. A study using the Behavioral Risk Factor Surveillance System (BRFSS) survey in 2012 reported that 64.2% of women aged 60 to 70 had received a screening mammogram over the past 12 months (Dehkordy et al., 2015). Though these results are higher than the proportions found in this study for women aged 65 to 74 years and 75+ years, the BRFSS survey was a self-report study that included Medicare Advantage patients and was subject to recall and selection biases via the telephone household survey.
Another study finding dissimilar results utilized the 5% random sample of Medicare claims and found the odds of screening mammograms increased after the ACA implementation (Cooper, Kou, Schluchter, Dor, & Koroukian, 2015). This study examined in-patient, out-patient, and physician claims and utilized the GEE analytic model. However, the analysis was not stratified into age groups per the USPSTF recommendations and used exclusively claims data. Also, the study by Cooper et al. (2015) examined years 2009 to 2012, only included women aged 70 years and over, and did not exclude for mastectomy.
Consistent with the results of our study, Jiang et al. (2015) utilized Medicare claims data and determined that rates of screening mammograms decreased in women aged 75 years and above after the 2009 revision to the USPSTF guideline, adjusting for age, race, geographic region, and socioeconomic status. However, decreases in screening mammogram utilization may not be attributable to USPSTF guidelines (Jiang et al., 2015) but rather physician specialty guidelines (Scheel et al., 2016). A previous study using the National Ambulatory Medical Care Survey (NAMCS) found decreased screening mammogram referrals from family and internal medicine specialties and no significant change among gynecologists and obstetricians (Scheel et al., 2016). Therefore, the decreased referrals among family and internal medicine physicians may be influenced by specialty society-specific guidelines of the American Academy of Family Physicians and the American College of Physicians rather than the USPSTF recommendation changes (Scheel et al., 2016). Further research of screening mammogram utilization by specialty guidelines for the physician who ordered the screening is warranted. In addition to changing specialty guidelines, previous studies have demonstrated that some physicians may be reluctant to implement the 2009 USPSTF recommendations in the general population due to changing patient preferences (Corbelli et al., 2014; Fedewa et al., 2016). These preferences, which may change among women as they age, include patient satisfaction, preference for a given physician specialty, and concerns about potential malpractice lawsuits (Corbelli et al., 2014; Haggerty et al., 2005; Meissner, Klabunde, Han, Benard, & Breen, 2011; Nutting et al., 2001; Shaneyfelt, Mayo-Smith, & Rothwangl, 1999).
One limitation of our study was that Hispanics, Asians, Native Americans, and multiracial women were not captured separately in our sample due to small sample size. Though our results do not reflect a diverse population of women, our results of the weighted sample are reflective of the general Medicare FFS population who qualified for Medicare due to age and did not include Medicare Advantage respondents (Cubanski et al., 2015). Another limitation of our study was that our sample was restricted to women aged 65 years and older. Therefore, we did not examine those aged 50 to 64 years who may also have been affected by the USPSTF recommendation changes. However, because women aged 65 years and over have an increased risk of breast cancer, this was a valid age group to analyze receipt of screening mammograms (American Cancer Society, 2013; Howlader et al., 2016).
This study is one of the first studies to demonstrate the relationship between the ACA implementation and screening mammograms in the Medicare population (Cooper et al., 2015). Another strength of this study is that the self-report survey questions contained potential confounders such as geographic location, ethnicity, and educational level, which are not found in claims data. Also, we utilized MCBS data linked to Medicare physician claims data to obtain screening procedures.
Despite the ACA implementation and expanded access for preventive services, screening mammograms have decreased in recent years. Future research as to why women are no longer receiving screening mammograms despite increased access from the ACA is warranted. It is also important to consider the changing USPSTF recommendations and physician specialty guidelines when assessing screening utilization.
Footnotes
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Laura M. Bozzi, M.S is funded by the NIA T32 AG00262.
