Disparities in the use of screening magnetic resonance imaging of the breast in community practice by race, ethnicity, and socioeconomic status
We thank the participating women, mammography facilities, and radiologists for the data they provided for the current study. A list of the Breast Cancer Surveillance Consortium investigators and procedures for requesting data for research purposes are provided at http://breastscreening.cancer.gov/.
Abstract
BACKGROUND
Uptake of breast magnetic resonance imaging (MRI) coupled with breast cancer risk assessment offers the opportunity to tailor the benefits and harms of screening strategies for women with differing cancer risks. Despite the potential benefits, there is also concern for worsening population-based health disparities.
METHODS
Among 316,172 women aged 35 to 69 years from 5 Breast Cancer Surveillance Consortium registries (2007-2012), the authors examined 617,723 negative screening mammograms and 1047 screening MRIs. They examined the relative risks (RRs) of MRI use by women with a <20% lifetime breast cancer risk and RR in the absence of MRI use by women with a ≥20% lifetime risk.
RESULTS
Among women with a <20% lifetime risk of breast cancer, non-Hispanic white women were found to be 62% more likely than nonwhite women to undergo an MRI (95% confidence interval, 1.32-1.98). Of these women, those with an educational level of some college or technical school were 43% more likely and those who had at least a college degree were 132% more likely to receive an MRI compared with those with a high school education or less. Among women with a ≥20% lifetime risk, there was no statistically significant difference noted with regard to the use of screening MRI by race or ethnicity, but high-risk women with a high school education or less were less likely to undergo screening MRI than women who had graduated from college (RR, 0.40; 95% confidence interval, 0.25-0.63).
CONCLUSIONS
Uptake of screening MRI of the breast into clinical practice has the potential to worsen population-based health disparities. Policies beyond health insurance coverage should ensure that the use of this screening modality reflects evidence-based guidelines. Cancer 2016;122:611–617. © 2015 American Cancer Society.
INTRODUCTION
Although mammography has been the cornerstone of breast cancer screening, advanced breast imaging technologies such as magnetic resonance imaging (MRI) coupled with breast cancer risk assessment algorithms provide greater opportunity to improve the balance of benefits and harms by tailoring screening strategies for subgroups of women with differing risks of developing breast cancer. Consistent with a risk-based screening approach, in 2007 the American Cancer Society (ACS) recommended that women at high risk of developing breast cancer (ie, a lifetime risk of ≥20%) should be screened annually with MRI in addition to mammography starting at age 30 years.1 For high-risk women, breast MRI has higher sensitivity than mammography for identifying cancer, but has modest specificity that leads to higher false-positive rates and additional workup, even among women with a higher risk of developing breast cancer.2-4 MRI is also more expensive; can trigger claustrophobia and anxiety for some women; and requires the use of intravenous gadolinium, with its associated risks. The use of screening MRI in community practice has been increasing over time, yet MRI may be used in excess of guidelines by those at average risk of developing breast cancer and “underused” by those at higher risk, in contrast to clinical guidelines.5, 6
Although there are well-documented disparities in screening mammography use,7-12 to our knowledge little is known regarding how racial, ethnic, and socioeconomic characteristics influence the use of advanced screening modalities such as MRI that are becoming increasingly available in community practice. The uptake of screening MRI in US radiologic practice has the potential to increase population-based health disparities by race, ethnicity, and socioeconomic status (SES). In particular, a lack of guideline-consistent use of MRI by high-risk, disadvantaged women may be associated with delayed diagnosis whereas the use of MRI in excess of guidelines by average-risk, more advantaged women may divert health care resources from more appropriate use and may expose women to unnecessary biopsies, anxiety from additional diagnostic workup, and the risks associated with gadolinium exposure.
The goal of the current study was to examine whether the use of screening MRI varies by race, ethnicity, and SES (as assessed by education), after accounting for lifetime risk of developing breast cancer, in community practice using data from the Breast Cancer Surveillance Consortium (BCSC). Because the use of MRI screening should be risk-based, differences in use by race, ethnicity, and SES after accounting for risk provide strong evidence for disparities in care.13 The use of MRI by women with a <20% lifetime risk of breast cancer in excess of guidelines could suggest “overuse,” whereas among women with a lifetime risk of ≥20%, a lack of guideline-consistent use of MRI screening could suggest “underuse.” As risk-based screening becomes more widely adopted in clinical practice, ensuring that each woman receives the most appropriate level of screening should promote both individual and population-level health.
MATERIALS AND METHODS
Study Registries
The BCSC is a consortium of breast imaging registries in community-based settings with linkages to tumor and/or pathology registries, and a centralized Statistical Coordinating Center (SCC). This study used data from 5 registries: the Carolina Mammography Registry, Group Health Cooperative (Washington state), New Hampshire Mammography Network, San Francisco Mammography Registry, and Vermont Breast Cancer Surveillance System.14 The data from these 5 registries reflect mammography and screening MRI practice as it is performed in the community.15 Each registry and the SCC received Institutional Review Board approval for either active consent or passive permission or a waiver of consent to enroll participants, link study data, and perform analytic studies. All registries and the SCC have received a federal Certificate of Confidentiality and other protection for the identities of the women, physicians, and facilities that were subjects of this research.
Study Population
We included women aged 35 to 69 years who had a negative screening mammogram (ie, to ensure that any subsequent MRI was not being performed for diagnostic purposes). The BCSC defines a negative screening mammogram as a Breast Imaging-Reporting and Data System (BI-RADS) final assessment of 1, 2, or 3 (with no recommendation for biopsy, fine-needle aspiration, or surgical consult).
At the time of breast imaging, women completed a questionnaire to ascertain age, race, ethnicity, level of education, first-degree family history of breast cancer, history of breast procedures, and other breast cancer risk factors. We excluded women with a prior history of breast cancer or ductal carcinoma in situ, or prior breast augmentation (because the sensitivity of mammography may be lower for these women, who therefore may opt for MRI for other reasons beyond risk16). We also excluded women for whom data with which to calculate the risk of breast cancer were missing (defined further below). Methods used to identify and assess screening mammograms, screening MRIs, patient characteristics, and outcomes have been described previously.5, 15, 17
Women were included if they received a mammogram in a BCSC registry from 2007 until 15 months before the most recent date of complete MRI imaging data capture available for each registry (Carolina Mammography Registry: December 31, 2012; San Francisco Mammography Registry: December 31, 2012; Vermont Breast Cancer Surveillance System: December 31, 2012; New Hampshire Mammography Network: September 30, 2010; and Group Health Cooperative: May 31, 2011). To avoid artificially underestimating the use of screening MRI by including facilities in which MRI was not readily available, we only included those women who underwent a mammogram at a facility participating in the BCSC that reported at least 5 MRI examinations during the study period.
Definition of Risk
The lifetime risk of developing breast cancer was calculated using the algorithm of Gail et al, which includes age, race, previous breast biopsy results, presence of atypia on any prior biopsy, age at menarche, age at first live birth, and history of breast cancer in first-degree relatives.18, 19 Lifetime risk was calculated on the basis of covariate values at the time of a woman's first screening mammogram during the study period. We defined women as being at high risk of developing breast cancer if their lifetime risk of breast cancer was ≥20% because guidelines suggest that these women should be screened annually by MRI in addition to mammography starting at age 30 years.1 We defined women as being at average risk if their lifetime risk of developing breast cancer was <20%.
Covariates
In addition to lifetime risk of breast cancer, the principal covariates in the current study were race and ethnicity (categorized as non-Hispanic white, non-Hispanic black, Hispanic, and other) and SES, as assessed by level of education (categorized as high school graduate or General Educational Development [GED] or less, some college or technical school, or college graduate or higher). We also examined age at the time of their first mammogram during the study period (categorized as 35-39 years, 40-49 years, 50-59 years, and 60-69 years) and year of first mammogram during the study period.
Outcome Assessment
For each woman, we included all the screening mammograms performed during the study period and then examined use of a screening MRI within 15 months of each screening mammogram (either before or after) to provide some allowance for scheduling given the annual recommendation. We conducted the primary analysis at the “woman level” by considering women to have received a screening MRI if an examination was documented within 15 months of any eligible mammogram. Women with no screening MRI examinations observed within 15 months of any screening mammogram were defined as nonusers. For high-risk women, for whom guidelines suggest receipt of an MRI, the lack of an MRI could be considered as potential “underuse.” For women at average risk, we considered receipt of a screening MRI to be evidence of potential “overuse.” As a secondary analysis, to examine trends in MRI use over time, we conducted an “examination-level” analysis, in which the outcome was the percentage of mammograms with an MRI performed within 15 months of their mammogram.
Statistical Analysis
We compared lifetime risk of breast cancer by patient race, ethnicity, and level of education. We then analyzed associations between the use of screening MRI and these patient characteristics separately for women with a lifetime risk of breast cancer of <20% and ≥20%. Relative risks (RRs), robust standard errors, and 95% confidence intervals (95% CIs) were estimated with modified Poisson regression using generalized estimating equations.20 Herein, we present 2 sets of models; the first adjusted only for registry and the second added adjustment for age at first mammogram during the study period, race/ethnicity, level of education, and year of first mammogram during the study period. Because of the small numbers of non-Hispanic black and Hispanic women (and a similar direction of association in these groups), the adjusted models compared non-Hispanic white versus nonwhite women (non-Hispanic black, Hispanic, and “other” race/ethnicity combined). To account for the number of mammograms observed in the BCSC data during the study period for each woman (women who received more mammograms had more opportunities to undergo an MRI), regression models included the number of mammograms as an offset term. For the secondary analysis examining trends in use over time, we used a modified Poisson regression model adjusted for BCSC registry applied to the examination-level data. Generalized estimating equations were used to address correlation among an individual woman's examinations. All analyses were performed using SAS statistical software (version 9.3; SAS Institute Inc, Cary, NC), and a 2-sided P<.05 was considered statistically significant.
RESULTS
Description of the Sample
The study sample included 316,172 women who underwent a screening mammogram during the study period; of these, 1047 women (0.3%) received a screening MRI (Table 1). The majority of women in the sample were aged 40 to 59 years at the time of the first mammogram included in the study. The majority of women (68.7%) described themselves as non-Hispanic white, 7.6% as non-Hispanic black, 6.6% as Hispanic, and 17.1% as being of other race/ethnicity (81.4% of this “other” group was Asian). Although the majority of women had at least a college degree, 20.9% had a high school degree (or its equivalent) or less, and 25.5% had some college or technical school beyond high school. High-risk women comprised 1.4% of the sample. Overall, only 6.2% of women (269 of 4358 women) with a ≥20% lifetime risk of breast cancer were observed to receive a screening MRI examination, and few women (777 of 311332 women; 0.3%) with a <20% risk were noted to receive a screening MRI examination. Of the 1047 women in the current study sample who underwent breast MRIs, 74.3% were women with a <20% risk of breast cancer.
| Characteristic | No. | % |
|---|---|---|
| No. of women | 316,172 | 100 |
| No. of women with breast MRI examination | 1047 | 0.33 |
| No. of mammograms | 617,723 | |
| Age at first examination during the study period, y | ||
| 35-39 | 14,025 | 4.4 |
| 40-49 | 114,206 | 36.1 |
| 50-59 | 113,327 | 35.8 |
| 60-69 | 74,614 | 23.6 |
| Race | ||
| Non-Hispanic white | 197,430 | 68.7 |
| Non-Hispanic black | 21,778 | 7.6 |
| Hispanic | 19,098 | 6.6 |
| Other | 49,193 | 17.1 |
| Level of education | ||
| ≤High school graduate/GED | 54,534 | 20.9 |
| Some college or technical school | 66,485 | 25.5 |
| ≥College graduate | 139,970 | 53.6 |
| Lifetime Gail risk of breast cancer | ||
| ≥20% | 4358 | 1.4 |
| <20% | 311,332 | 98.6 |
| Use of breast MRI | ||
| ≥20% | 269 | 6.2 |
| <20% | 777 | 0.3 |
- Abbreviations: GED, General Educational Development; MRI, magnetic resonance imaging.
- a Race/ethnicity data were missing for 28,673 individuals, data regarding level of education were missing for 55,183 individuals, and data regarding lifetime risk of breast cancer were missing for 482 individuals.
Lifetime Risk of Breast Cancer by Sociodemographic Characteristics
A higher percentage of non-Hispanic white women in the current study sample had a lifetime risk of breast cancer of ≥20% compared with non-Hispanic black or Hispanic women (1.9%, 0.1%, and 0.6%, respectively). Women with at least some college education were also slightly more likely to have a risk of breast cancer of ≥20% compared with women who had a high school education or less (1.6% vs 1.3%).
Use of MRI by Women With a Lifetime Risk of <20%
Among those women at average risk, non-Hispanic white women were 69% more likely than non-Hispanic black women (RR, 1.69; 95% CI, 1.11-2.57) to undergo screening MRI (Table 2). There were no differences in MRI use noted between Hispanic or other nonwhite women and non-Hispanic black women. After adjustment for race, level of education, age at first examination during study period, and examination year in addition to registry, non-Hispanic white women were found to be 62% more likely than nonwhite women to receive a screening MRI (RR, 1.62; 95% CI, 1.32-1.98). Average-risk women who had at least a college education were 132% more likely than women with a high school education or less (RR, 2.32; 95% CI, 1.76-3.06 after adjustment) and 43% more likely than those with some college education to undergo a screening MRI (for women with a high school education or less compared with those with at least a college education: RR, 1.43; 95% CI, 1.04-1.96).
| Characteristic | RRa | 95% CI | RRb | 95% CI | ||
|---|---|---|---|---|---|---|
| Race | ||||||
| Non-Hispanic white | 1.69 | (0.11-2.57) | 1.62 | (1.32-1.98) | ||
| Non-Hispanic black | 1.00 | - | - | |||
| Hispanic | 0.95 | (0.56-1.60) | ||||
| Other | 0.88 | (0.56-1.39) | ||||
| Non-white | 1.00 | - | - | |||
| Level of Education | ||||||
| ≤High school graduate/GED | 1.00 | - | - | 1.00 | - | - |
| Some college or technical school | 1.63 | (1.19-2.23) | 1.43 | (1.04-1.96) | ||
| ≥College graduate | 3.04 | (2.33-3.96) | 2.32 | (1.76-3.06) | ||
- Abbreviations: 95% CI, 95% confidence interval; GED, General Educational Development; MRI, magnetic resonance imaging; RR, relative risk.
- a Adjusted for registry.
- b Adjusted for race, level of education, age at first examination, examination year, and registry.
Use of Screening MRI by Women With a Lifetime Risk of ≥20%
Among women with a lifetime risk of breast cancer of ≥20%, there was no statistically significant difference in the use of screening MRI noted by race or ethnicity (Table 3). High-risk women who had a high school education or less were 60% less likely to receive screening MRI compared with those who had graduated from college (RR, 0.40; 95% CI, 0.25-0.63 after adjustment). There was also a similar trend noted for women with some college education but who had not graduated (RR, 0.81; 95% CI, 0.60-1.09 after adjustment).
| Characteristic | RRa | 95% CI | RRb | 95% CI | ||
|---|---|---|---|---|---|---|
| Race | ||||||
| Non-Hispanic white | 1.00 | - | - | 1.00 | - | - |
| Non-Hispanic black | - | - | - | - | - | - |
| Hispanic | 0.87 | (0.36-2.11) | - | - | - | |
| Other | 0.72 | (0.39-1.33) | 0.73 | (0.44-1.21) | ||
| Level of education | ||||||
| ≤High school graduate/GED | 0.34 | (0.22-0.55) | 0.40 | (0.25-0.63) | ||
| Some college or technical school | 0.76 | (0.56-1.02) | 0.81 | (0.60-1.09) | ||
| ≥College graduate | 1.00 | - | - | 1.00 | - | - |
- Abbreviations: 95% CI, 95% confidence interval; GED, General Educational Development; MRI, magnetic resonance imaging; RR, relative risk.
- a Adjusted for registry.
- b Adjusted for race, level of education, age at first examination, examination year, and registry.
Use of Screening MRI Over Time
As a secondary analysis, performed at the “examination level” instead of the “woman level” to examine trends in MRI use over time, we found a significant increase in the use of screening MRI from 2008 onward (Table 4). The RR of undergoing a screening MRI in 2011 compared with 2007 was 1.25 (95% CI, 1.05-1.48).
| Year | Adjusted RRa | 95% CI | P |
|---|---|---|---|
| 2007 | - | ||
| 2008 | 0.88 | 0.76-1.03 | .0001 |
| 2009 | 0.95 | 0.81-1.10 | |
| 2010 | 1.13 | 0.97-1.31 | |
| 2011 | 1.25 | 1.05-1.48 |
- Abbreviations: 95% CI, 95% confidence interval; MRI, magnetic resonance imaging; RR, relative risk.
- a Adjusted for registry.
DISCUSSION
The uptake of screening MRI of the breast into US clinical practice has the potential to increase population-based health disparities by race, ethnicity, and SES. The absence of MRI screening in high-risk, disadvantaged women may be associated with delayed diagnosis, and the use of screening MRI in excess of guidelines by average-risk, more advantaged women may divert health care resources from more appropriate use on a population level and expose individual women to associated harms, including false-positive test results, unnecessary diagnostic workup, and benign biopsies. The results of the current study indicate that there has been an increase in the use of screening MRI between 2007 and 2011 and confirms that there is broad underuse of MRI by high-risk women. However, we believe the current study goes beyond prior work to demonstrate that among high-risk women, women with lower educational attainment are less likely to undergo screening MRI compared with women with at least a college education.5, 6 The current study also found evidence of the use of screening MRI in excess of guidelines by average-risk women because this group received the majority of screening MRIs in the study population. The current study results further suggest that average-risk women with at least a college education were more likely to receive a screening MRI in excess of guidelines than women with less education and that non-Hispanic white women were more likely to undergo a screening MRI in excess of guidelines than nonwhite women. Consistent with prior studies, we found that white women and women with more education were, on average, at a higher risk of breast cancer, perhaps because of differences in reproductive and lifestyle risk factors.21 It is important to note that the current study analyses of MRI use accounted for differences in risk. Further study should examine potential causes of the observed disparities, which may include patient preference, provider-level variation in recommending and ordering screening MRI, patient-provider communication, or financial barriers to care.
Although many studies have documented disparities in the use of mammography,12, 22, 23 to the best of our knowledge the current study is one of the first to directly examine risk-based differences in the use of breast cancer screening with MRI by race, ethnicity, and education. Other studies have found that high-risk women have low overall rates of adherence to the ACS guideline recommendation for screening MRI,24 most likely because it was not recommended by a health provider; women did not realize that they were high risk; or the women were restricted by claustrophobia, costs, or time constraints.25 The current study findings of disparities in MRI use by high-risk women are supported by earlier studies that suggest that women screened with MRI were more likely than women screened by mammography alone to be white.5 A study using self-reported data from the 2010 National Health Interview Survey found that 2% of women, independent of risk, reported having undergone an MRI within the previous 2 years, most often for diagnostic evaluation.26 That study did not report differences in screening MRI use by race, ethnicity, or education, and differs from the results of the current study with regard to its finding that non-Hispanic black women were more likely than white women to receive MRI for any indication (ie, screening or diagnostic).26
The results of the current study highlight the importance of educating all women about their breast cancer risk so that high-risk women can receive recommended screening and average-risk women can avoid unnecessary test use. Although clinicians frequently do not perform breast cancer risk assessment,27 more advantaged women may be more likely to discuss their risk of breast cancer with a physician or perceive their cancer risk to be higher due to family history.28 As we learn more about risk-based screening, we will need to develop systems-based solutions and tools to help providers and patients assess risk to promote informed decision-making. With the dissemination of advanced imaging technology for breast cancer screening, one challenge is to get the right test to the right woman. For example, income inequality in the local area in which a woman lives may affect the diffusion of new technologies such as MRI and contribute to disparities in use.29 The current study results inform technology use at a population level, which is a timely goal given the emphasis on comparative effectiveness in national health care reform. If an increasing percentage of the approximately 39 million mammography examinations performed each year are supplemented by MRI, the associated costs will be substantial. In 2013, a screening mammogram cost approximately $150 whereas the price range for MRI was $880 to $1627.30 The increased complexity of risk-based screening protocols places greater demands on health care systems to implement screening guidelines.31 Tools for informed decision-making should be accessible to all patients, and payers should be required to pay for risk-appropriate screening.
The current study has several limitations. We used the model of Gail et al to assess breast cancer risk. Although the ACS guidelines recommend that risk assessment be performed using a family history-focused model (ie, the Tirer-Cuzick Breast Cancer Risk Assessment model and the Claus model),1 the model of Gail et al is more widely accessible to patients and providers and may be an important first step toward risk assessment in primary care. Even among the family history-based models, there are important inconsistencies in the assessment of individual women.32 Some women with lifetime breast cancer risk scores of <20% based on the model of Gail et al may have an indication for screening MRI that was not captured in the current study data (eg, BRCA mutation, first-degree relative with a BRCA mutation, or prior chest radiotherapy). However, it is unlikely that these risk factors account for a substantial percentage of the women with a <20% risk undergoing screening MRI. The relatively small number of non-Hispanic black and Hispanic women in the current study sample limited our ability to examine these groups separately in the adjusted models. The current analysis was limited to examinations performed in facilities that participate in the BCSC. Women enter and leave the registry based on where they receive their breast imaging. The majority of women were not under observation for the entire study period. In addition, some of the facilities only participated in the BCSC for part of the study period. Some women who underwent a screening mammogram at a facility that participates in the BCSC may have received a screening MRI at a nonparticipating facility. By limiting the analysis to facilities that performed both mammography and MRI, we minimized the potential source of underestimation of MRI use. However, we were not able to estimate the actual prevalence of MRI use. For this reason, the current analysis was primarily focused on RR estimates that were unbiased even with incomplete capture of MRIs.33 Although guidelines recommend annual screening, we were unable to examine this because we had limited longitudinal data concerning individual women. Despite these limitations, we believe the current study sample is one of the few that can examine risk-based disparities in the use of screening MRI in community practice using self-reported information regarding race, ethnicity, and level of education and record-based indications for examination that allowed us to include MRI examinations performed for screening purposes.
Optimal breast cancer screening and prevention will occur only if advanced screening technologies are translated into clinical practice in evidence-based, equitable ways. The broad dissemination of electronic health records offers opportunities for more explicit risk calculation and presentation in clinical practice. Systems-based solutions to risk assessment as well as tools for informed decision-making that are accessible to diverse populations are needed to ensure that the dissemination of advanced imaging does not contribute to health disparities or put added strain on limited health care resources.
FUNDING SUPPORT
Supported by the National Cancer Institute-funded Breast Cancer Surveillance Consortium (grant P01 CA154292 and grant HHSN261201100031C) and a National Cancer Institute grant (U54 CA163303). The collection of Breast Cancer Surveillance Consortium cancer and vital status data used in the current study was supported in part by several state public health departments and cancer registries. For a full description of these sources, see http://breastscreening.cancer.gov/work/acknowledgment.html. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Cancer Institute or the National Institutes of Health. The funder did not participate in the design of the study; collection, management, analysis, and interpretation of the data; or preparation, review, or approval of the article.
CONFLICT OF INTEREST DISCLOSURES
Christoph I. Lee was supported in part by American Cancer Society grant 126947-MRSG-14-160-01-CPHPS for work performed as part of the current study and has also received a research grant and consulting fees from GE Healthcare for work performed outside of the current study. Natasha K. Stout was supported in part by American Cancer Society grant 118223-MRSG-10-002-01-CPHPS for work performed as part of the current study.
