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Addressing Disparities Related to Access of Multimodality Breast Imaging Services Before and During the COVID-19 Pandemic

Published:March 24, 2022DOI:https://doi.org/10.1016/j.acra.2022.03.017
      Despite technological advancements focused on reducing breast cancer mortality through early detection, there have been reported disparities in the access to these imaging services with underserved patient populations (including racial minority groups and patients of low socioeconomic status) showing underutilization compared to other patient groups. These underserved populations tend to have more advanced breast cancer presentations, in part due to delays in diagnosis resulting in later stage of disease presentation. To make matters worse, the COVID-19 pandemic declared in March 2020 has resulted in significant healthcare disruptions leading to extensive delays in breast imaging services which are expected to negatively impact breast cancer mortality long-term. Given the worsening disparity in breast cancer mortality among racial/ethnic minorities and financially disadvantaged groups, it is vital to address these disparity gaps with the goal of reducing the barriers to timely breast cancer diagnosis and addressing breast cancer mortality differences among breast cancer patients. Therefore, this review aims to provide a discussion highlighting the disparities related to breast imaging access, the effects of the COVID-19 pandemic on these disparities, current targeted interventions implemented in breast imaging practices to reduce these disparities, and future directions on the journey to reducing disparity gaps for breast imaging patients. Tackling the root cause factors of the persistent breast cancer-related disparities is critical to meeting the needs of patients who are disadvantaged and can lead to continued improvement in the quality of individualized care for patients who have higher breast cancer morbidity and mortality risks.

      Key Words

      INTRODUCTION

      Breast cancer is the most common cause of non-cutaneous-related cancer and the second leading cause of cancer-related death in women (

      American Cancer Society. How common is breast cancer? Available at: https://www.cancer.org/cancer/breast-cancer/about/how-common-is-breast-cancer.html. Accessed on December 6, 2021.

      ). It is estimated that in 2021, over 330,000 new cases of breast cancer were diagnosed and about 44,000 deaths resulted from breast cancer (

      American Cancer Society. How common is breast cancer? Available at: https://www.cancer.org/cancer/breast-cancer/about/how-common-is-breast-cancer.html. Accessed on December 6, 2021.

      ). Since 2007, mortality related to breast cancer has been steadily decreasing due to interventions aimed towards early detection, increased awareness, and advancements in diagnosis and treatment (

      American Cancer Society. How common is breast cancer? Available at: https://www.cancer.org/cancer/breast-cancer/about/how-common-is-breast-cancer.html. Accessed on December 6, 2021.

      ). Breast cancer morbidity and mortality rates, however, are not equal in incidence and distribution across all racial and ethnic backgrounds, with negative trends skewing more towards racial minority women compared to White women (
      • DeSantis CE
      • Fedewa SA
      • Goding Sauer A
      • et al.
      Breast cancer statistics, 2015: convergence of incidence rates between Black and White women.
      ,
      • Li CI.
      Racial and ethnic disparities in breast cancer stage, treatment and survival in the United States.
      ,
      • Vernon SW
      • Tilley BC
      • Neale AV
      • et al.
      Ethnicity, survival, and delay in seeking treatment for symptoms of breast cancer.
      ,
      • Noone AM
      • Howlader N
      • Krapcho M
      • et al.
      Table 4.18. Cancer of the female breast (invasive): Age-adjusted rates and trends by race/ethnicity, 2011-2015.
      ). Additionally, the breast cancer 5-year survival among Black, Hispanic, and Native American women is lower than White women (
      • Li CI.
      Racial and ethnic disparities in breast cancer stage, treatment and survival in the United States.
      ,
      • Vernon SW
      • Tilley BC
      • Neale AV
      • et al.
      Ethnicity, survival, and delay in seeking treatment for symptoms of breast cancer.
      ,
      • Ooi SL
      • Martinez ME
      • Li CI.
      Disparities in breast cancer characteristics and outcomes by race/ethnicity.
      ). The cause of these disparities among distinct racial and ethnic groups is thought to be multifactorial, is due to a combination of advanced stage at the time of breast cancer detection and poorer state-specific survival rates, and is influenced by a multitude of factors related to low socioeconomic status (SES), social injustice and cultural barriers (
      • Freeman HP
      • Chu KC.
      Determinants of cancer disparities: barriers to cancer screening, diagnosis, and treatment.
      ,
      • Perez-Stable EJ
      • Afable-Munsuz A.
      • Kaplan CP
      • et al.
      Factors influencing time to diagnosis after abnormal mammography in diverse women.
      ,
      • Jones BA
      • Daily A
      • Calvocoressi L
      • et al.
      Inadequate follow-up of abnormal screening mammograms: findings from the race differences in screening mammography process study (United States).
      ,
      • Syed ST
      • Gerber BS
      • Sharp LK.
      Traveling towards disease: transportation barriers to health care access.
      ). Furthermore, prior research showed that racial minority and low SES women had less interest in knowing their breast cancer risk compared to White and higher income women (
      • Amornsiripanitch N
      • Ameri SM
      • Goldberg RJ.
      Impact of age, race, and socioeconomic status on women's perceptions and preferences regarding communication of estimated breast cancer risk.
      ). Therefore, these barriers to breast cancer diagnosis and access can increase the likelihood for at-risk populations to be vulnerable to more aggressive presentations and advanced stage of disease at the time of diagnosis (
      • Perez-Stable EJ
      • Afable-Munsuz A.
      • Kaplan CP
      • et al.
      Factors influencing time to diagnosis after abnormal mammography in diverse women.
      ,
      • Jones BA
      • Daily A
      • Calvocoressi L
      • et al.
      Inadequate follow-up of abnormal screening mammograms: findings from the race differences in screening mammography process study (United States).
      ,
      • Syed ST
      • Gerber BS
      • Sharp LK.
      Traveling towards disease: transportation barriers to health care access.
      ).
      Advancements in technology during the last decade such as digital breast tomosynthesis (DBT) and breast MRI have increased the likelihood of earlier detection of breast cancer, thus resulting in lower stage of disease at the time of diagnosis (
      • Lee CI
      • Bogart A
      • Germino JC
      • et al.
      Availability of advanced breast imaging at screening facilities serving vulnerable populations.
      ). However, it has been established that minority and low SES patients are typically the last to benefit from these advancements (
      • Groeneveld PW
      • Laufer SB
      • Garber AM.
      Technology diffusion, hospital variation, and racial disparities among elderly Medicare beneficiaries: 1989–2000.
      ,
      • Onega T
      • Duell EJ
      • Shi X
      • et al.
      Race versus place of service in mortality among medicare beneficiaries with cancer.
      ). This can be attributed to multifactorial logistical barriers including limited available appointments that can make it challenging for these patients to find an appointment time that works with their individual and family schedule logistics, limited available services in certain areas such as more rural parts of the nation, and higher co-pay and out-of-pocket costs for services without vouchers or government assistance (
      • Berg WA.
      Tailored supplemental screening for breast cancer: what now and what next?.
      ).
      Exacerbating the current climate, the COVID-19 pandemic declared in March 2020 has resulted in significant disruptions in the workflow for breast imaging practices nationwide (

      Society of Breast Imaging. Statement on Breast Imaging during the COVID-19 Pandemic. Available at: https://www.sbi-online.org/Portals/0/Position%20Statements/2020/society-of-breast-imaging-statement-on-breast-imaging-during-COVID19-pandemic.pdf. Accessed on December 6, 2021.

      ). This resulted in extensive delays in breast imaging appointments and breast cancer treatment, which are expected to have long-term negative impacts on breast cancer mortality by 2030 (
      • Papautsky EL
      • Hamlish T.
      Patient-reported treatment delays in breast cancer care during the COVID-19 pandemic.
      ,
      • Alagoz O
      • Lowry KP
      • Kurian AW
      • et al.
      Impact of the COVID-19 pandemic on breast cancer mortality in the US: estimates from collaborative simulation modeling.
      ). Racial minority and low SES patients were especially hit hard by the COVID-19 pandemic as preliminary data have demonstrated that these populations are not recovering from the initial delays as well as other patient groups, resulting in many patients becoming lost to follow-up which potentially increases their risk of an advanced stage breast cancer diagnosis (
      • Sprague BL
      • Lowry KP
      • Milioretti DL
      • et al.
      Changes in mammography utilization by women's characteristics during the first 5 months of the COVID-19 pandemic.
      ,
      • Miller MM
      • Meneveau MO
      • Rochman CM
      • et al.
      Impact of the COVID-19 pandemic on breast cancer screening volumes and patient screening behaviors.
      ). Thus, the COVID-19 pandemic has actually worsened disparities related to patient access of breast imaging services and breast cancer treatment.
      Given the growing disparity in breast cancer mortality among racial, ethnic, and financially disadvantaged groups, it is vital to address these disparity gaps with the goal of reducing the barriers faced by racial minority patients, in order to improve breast cancer survival outcomes for all patients. Currently, there is a sparsity of literature on disparities related to the impact of lack of access to breast imaging resources and the compounding effect of the COVID-19 pandemic on this. This review aims to provide a discussion highlighting the disparities related to the unique workflow employed in breast imaging, the effects of the COVID-19 pandemic on these disparities, current targeted interventions implemented in breast imaging practices to reduce these disparities, and future directions on the journey of reducing disparity gaps for breast imaging patients who are underserved.

      DISPARITIES IN BREAST IMAGING RESOURCES – SCREENING MAMMOGRAPHY

      The utilization of screening mammography has been a major contributor to the reduction in breast cancer mortality via the early detection of breast cancer, especially in women who undergo consistent annual screening mammography (
      • Duffy SW
      • Tabar L
      • AMF Y
      • et al.
      Beneficial effects of consecutive screening mammography examination on mortality from breast cancer: a prospective study.
      ). To make screening mammography more accessible, cost-sharing for insured patients has been largely eliminated and there are typically no out-of-pocket costs for patients who have private insurance or Medicare (
      • Nguyen DL
      • Harvey SC
      • Oluyemi E
      • Meyers KS
      • Mullen LA
      • Ambinder EB.
      Impact of improved screening mammography recall lay letter readability on patient follow-up.
      ,

      Medicare Mammograms. Available at: medicare.gov/coverage/mammograms. Accessed December 29, 2021.

      ,

      Kaiser Family Foundation. Coverage of Breast Cancer Screening and Prevention Services. Available at: https://www.kff.org/womens-health-policy/fact-sheet/coverage-of-breast-cancer-screening-and-prevention-services/. Accessed December 29, 2021.

      ). For patients without insurance, there are organizations such as the Susan G. Komen Breast Cancer Foundation which offer vouchers so that these patients can undergo screening mammography without out-of-pocket costs (
      • Nguyen DL
      • Harvey SC
      • Oluyemi E
      • Meyers KS
      • Mullen LA
      • Ambinder EB.
      Impact of improved screening mammography recall lay letter readability on patient follow-up.
      ,

      Medicare Mammograms. Available at: medicare.gov/coverage/mammograms. Accessed December 29, 2021.

      ,

      Kaiser Family Foundation. Coverage of Breast Cancer Screening and Prevention Services. Available at: https://www.kff.org/womens-health-policy/fact-sheet/coverage-of-breast-cancer-screening-and-prevention-services/. Accessed December 29, 2021.

      ). Despite these efforts, barriers still persist which prevent patients from obtaining the care they need. Black, Hispanic, and Asian populations have been shown to have lower likelihood of undergoing annual screening mammography when compared to White populations (
      • Ahmed AT
      • Welch BT
      • Brinjikji W
      • et al.
      Racial disparities in screening mammography in the united states: a systematic review and meta-analysis.
      ,
      • Advani P
      • Advani S
      • Nayak P
      • et al.
      Racial/ethnic disparities in use of surveillance mammogram among breast cancer survivors: a systematic review.
      ,
      • Field TS
      • Doubeni C
      • Fox MP
      • et al.
      Under utilization of surveillance mammography among older breast cancer survivors.
      ). For Black populations, this was present for all age groups > 40 years and for Hispanic populations from age 40-65 years (
      • Ahmed AT
      • Welch BT
      • Brinjikji W
      • et al.
      Racial disparities in screening mammography in the united states: a systematic review and meta-analysis.
      ).
      The underlying etiology of the barriers to screening mammography access for underserved patients is suspected to be multifactorial (
      • Miller BC
      • Bowers JM
      • Payne JB
      • et al.
      Barriers to mammography screening among racial and ethnic minority women.
      ). Among these patient populations, the most common reported barrier is psychological/knowledge-related with specific focuses for each patient population (
      • Miller BC
      • Bowers JM
      • Payne JB
      • et al.
      Barriers to mammography screening among racial and ethnic minority women.
      ). Common to all groups was fear including, fear of breast cancer diagnosis, concern about side effects from the mammogram examination, and misinformation related to benefits/risks of screening mammography and national screening guidelines. For Black and Asian populations, prioritization of other responsibilities such as work and family and embarrassment/discomfort of male providers were unique barriers reported. For Black and Hispanic populations, procrastination which commonly manifested as delaying their appointment to the point of never going to it was a specific barrier reported. Cultural barriers that were specific to Asian, Muslim, and Hispanic populations included differences in primary language which prevented effective communication with providers and body modesty as the process of mammography requires exposure of the patient's breast which may be regarded as invasive in light of the cultural norms of these populations (
      • Miller BC
      • Bowers JM
      • Payne JB
      • et al.
      Barriers to mammography screening among racial and ethnic minority women.
      ,
      • Islam N
      • Patel S
      • Brooks-Griffin Q
      • et al.
      Understanding barriers and facilitators to breast and cervical cancer screening among Muslim women in NEW YORK city: perspective from key informants.
      ,
      • Azhar S
      • Wyatt LC
      • Jokhakar V
      • et al.
      Associations between spiritual health locus of control, perceived discrimination and breast and cervical cancer screening for muslim american women in New York city.
      ). Furthermore, logical aspects of annual screening mammography such as facility location and access to transportation preferentially negatively affects Black and Hispanic populations more than White populations (
      • Miller BC
      • Bowers JM
      • Payne JB
      • et al.
      Barriers to mammography screening among racial and ethnic minority women.
      ,
      • Peipins LA
      • Graham S
      • Young R
      • et al.
      Time and distance barriers to mammography facilities in the Atlanta metropolitan area.
      ). Longer travel distance to screening mammography facilities can detract time from work, family or other responsibilities which may hinder the ability of these patients to attend their appointment and further contributes to the likelihood of procrastination of medical appointments. For example, Peipins et al. in 2011 found that the median public transportation travel time was three times longer for Black populations compared to White populations and even with private transportation travel, Blacks still experienced longer travel times compared to Whites (
      • Peipins LA
      • Graham S
      • Young R
      • et al.
      Time and distance barriers to mammography facilities in the Atlanta metropolitan area.
      ). In addition, American Indian and Alaska native patients are the most disadvantaged when it comes to geographic access to screening mammography facilities as these populations tend to live in rural areas and have travel times two to three times longer compared to other racial/ethnic groups which has resulted in the lowest screening adherence rates (
      • Giuliano A
      • Papenfuss M
      • de Guernsey de Zapien J
      • et al.
      Breast cancer screening among Southwest American Indian women living on-reservation.
      ,
      • Roubidoux MA
      • Kaur JS
      • Rhoades DA.
      Health disparities in cancer among American Indians and Alaska natives.
      ). This is impactful as both these patient populations have higher breast cancer mortality rates similar to other minority groups compared to non-Hispanic White women and while other minority groups experienced a decline in mortality rates between 2013 and 2017, American Indian and Alaska native patients did not (
      • Roubidoux MA
      • Kaur JS
      • Rhoades DA.
      Health disparities in cancer among American Indians and Alaska natives.
      ). Therefore, it isn't surprising that increased mortality and advanced stage of breast cancer diagnosis unfortunately occur in these populations as a result of multilevel factors resulting in reduction of annual screening mammography adherence (
      • DeSantis CE
      • Fedewa SA
      • Goding Sauer A
      • et al.
      Breast cancer statistics, 2015: convergence of incidence rates between Black and White women.
      ,
      • Li CI.
      Racial and ethnic disparities in breast cancer stage, treatment and survival in the United States.
      ,
      • Vernon SW
      • Tilley BC
      • Neale AV
      • et al.
      Ethnicity, survival, and delay in seeking treatment for symptoms of breast cancer.
      ).
      Since the incorporation of digital breast tomosynthesis (DBT) in 2011, the use of DBT has led to increased cancer detection rates and overall reduction in recall rates with screening mammography (
      • De Munck L
      • de Bock GH
      • Otter R
      • et al.
      Digital vs screen-film mammography in population-based breast cancer screening: performance indicators and tumour characteristics of screen-detected and interval cancers.
      ,
      • Sharpe RE
      • Venkataraman S
      • Phillips J
      • et al.
      Increased cancer detection rate and variations in the recall rate resulting from implementation of 3D digital breast tomosynthesis into a population-based screening program.
      ). This benefit is only applicable to those who are able to undergo DBT instead of full field digital mammography (FFDM). Compared to FFDM, DBT has out-of-pocket costs with some insurance plans, thus inherently posing a barrier to access (
      • Falomo E
      • Myers K
      • Reichel KF
      • et al.
      Impact of insurance coverage and socioeconomic factors on screening mammography patients’ selection of digital breast tomosynthesis versus full-field digital mammography.
      ). Falomo et al. in 2018 showed that patients who chose DBT were significantly more likely to have insurance coverage, higher income, and higher education levels than patients who chose FFDM (
      • Falomo E
      • Myers K
      • Reichel KF
      • et al.
      Impact of insurance coverage and socioeconomic factors on screening mammography patients’ selection of digital breast tomosynthesis versus full-field digital mammography.
      ). Patients who chose FFDM compared to DBT reported difference in cost as the reason as most of these patients did not have insurance coverage (
      • Falomo E
      • Myers K
      • Reichel KF
      • et al.
      Impact of insurance coverage and socioeconomic factors on screening mammography patients’ selection of digital breast tomosynthesis versus full-field digital mammography.
      ). In fact, most patients who chose FFDM reported that if DBT was covered by insurance, they would be more likely to choose it (
      • Falomo E
      • Myers K
      • Reichel KF
      • et al.
      Impact of insurance coverage and socioeconomic factors on screening mammography patients’ selection of digital breast tomosynthesis versus full-field digital mammography.
      ). Lee et al. in 2021 showed that Black, Hispanic, and Asian populations have less access to DBT compared to White populations (
      • Lee CI
      • Zhu W
      • Onega T
      • et al.
      Comparative access to and use of digital breast tomosynthesis screening by women's race/ethnicity and socioeconomic status.
      ). Thus, access to advancements in screening technology appears to be lagging or absent for certain minority groups, thus diminishing the ability of these patient populations to experience the health benefits of improved screening technology (
      • Falomo E
      • Myers K
      • Reichel KF
      • et al.
      Impact of insurance coverage and socioeconomic factors on screening mammography patients’ selection of digital breast tomosynthesis versus full-field digital mammography.
      ).

      DISPARITIES IN BREAST IMAGING RESOURCES – SCREENING ULTRASOUND

      Women with dense breast tissue face unique challenges related to their breast density as not only do these patients have an innately higher risk of developing breast cancer, but also screening mammography has a lower sensitivity of breast cancer detection in these women compared to women with non-dense breast tissue (
      • Thigpen D
      • Kappler A
      • Brem R.
      The role of ultrasound in screening dense breasts-a review of the literature and practical solutions for implementation.
      ). As such, supplemental screening breast ultrasound has been shown to be useful for detecting additional breast cancers that are mammographically occult in this patient population, although there is the risk of false positive results (
      • Thigpen D
      • Kappler A
      • Brem R.
      The role of ultrasound in screening dense breasts-a review of the literature and practical solutions for implementation.
      ). However, unlike with screening mammography, screening breast ultrasound has associated out-of-pocket costs (
      Discuss Your Options
      BREM.
      ). Ezratty et al. in 2020 found that non-Hispanic Black and Hispanic women were not only less likely to be recommended for supplemental screening breast ultrasound, but also less likely to undergo the examination even if ordered compared to non-Hispanic White women (
      • Ezratty C
      • Vang S
      • Brown J
      • et al.
      Racial/ethnic differences in supplemental imaging for breast cancer screening in women with dense breasts.
      ). This implies that just as with diagnostic mammography, racial and financial barriers exist with the use of supplemental screening breast ultrasound, which prevent this subset of women with even higher risk of breast cancer from accessing this modality for supplemental screening for mammographically occult cancers.

      DISPARITIES IN BREAST IMAGING RESOURCES – DIAGNOSTIC MAMMOGRAPHY

      In the setting of an abnormal screening mammogram, prompt and consistent follow-up with diagnostic mammography is vital to maintaining lower breast cancer mortality (
      • Miller-Kleinhenz JM
      • Collin LJ
      • Seidel R
      • et al.
      Racial disparities in diagnostic delay among women with breast cancer.
      ). Delays in diagnostic mammography appointments of at least 6 weeks are significantly associated with increased breast cancer mortality (
      • Miller-Kleinhenz JM
      • Collin LJ
      • Seidel R
      • et al.
      Racial disparities in diagnostic delay among women with breast cancer.
      ,
      • Goldman LE
      • Walker R
      • Hubbard R
      • et al.
      Timeliness of abnormal screening and diagnostic mammography follow-up at facilities serving vulnerable women.
      ). Race/ethnicity was found to be a significant predictor in delays in diagnosis after an abnormal screening mammogram (
      • Jones BA
      • Daily A
      • Calvocoressi L
      • et al.
      Inadequate follow-up of abnormal screening mammograms: findings from the race differences in screening mammography process study (United States).
      ,
      • Miller-Kleinhenz JM
      • Collin LJ
      • Seidel R
      • et al.
      Racial disparities in diagnostic delay among women with breast cancer.
      ,
      • Goldman LE
      • Walker R
      • Hubbard R
      • et al.
      Timeliness of abnormal screening and diagnostic mammography follow-up at facilities serving vulnerable women.
      ,
      • Ramirez AG
      • Pérez-Stable EJ
      • Talavera GA
      • et al.
      Time to definitive diagnosis of breast cancer in Latina and non-Hispanic White women: the six cities study.
      ,
      • Nguyen KH
      • Pasick RJ
      • Stewart SL
      • et al.
      Disparities in abnormal mammogram follow-up time for Asian women compared with non-Hispanic White women and between Asian ethnic groups.
      ,
      • Press R
      • Carrasquillo O
      • Sciacca RR
      • et al.
      Racial/ethnic disparities in time to follow-up after an abnormal mammogram.
      ,
      • Gorin SS
      • Heck JE
      • Cheng B
      • et al.
      Delays in breast cancer diagnosis and treatment by racial/ethnic group.
      ). Within the last decade, multiple studies have demonstrated that Black, Hispanic, and Asian populations all experienced longer delays in diagnosis compared to White Non-Hispanic patients, with Black and Hispanic patients approaching or surpassing the 6-week timeframe cut-off (
      • Miller-Kleinhenz JM
      • Collin LJ
      • Seidel R
      • et al.
      Racial disparities in diagnostic delay among women with breast cancer.
      ,
      • Ramirez AG
      • Pérez-Stable EJ
      • Talavera GA
      • et al.
      Time to definitive diagnosis of breast cancer in Latina and non-Hispanic White women: the six cities study.
      ,
      • Nguyen KH
      • Pasick RJ
      • Stewart SL
      • et al.
      Disparities in abnormal mammogram follow-up time for Asian women compared with non-Hispanic White women and between Asian ethnic groups.
      ).
      The out-of-pocket costs associated with diagnostic mammography may be a contributing factor to disparities in the adherence to diagnostic mammography follow-up. Depending on location, the average cost of a diagnostic mammogram is $290 without insurance, which can be increased to a total of $540 if a breast and/or axillary ultrasound is also performed during the diagnostic appointment (
      Discuss Your Options
      BREM.
      ). Given this cost, patients within the most disadvantaged 15% of neighborhoods and with Medicare/Medicaid were found to be less likely to adhere to diagnostic imaging recommendations following an abnormal screening mammogram, compared to patients not in disadvantaged neighborhoods and those with private/commercial insurance (
      • Nguyen DL
      • Harvey SC
      • Oluyemi E
      • Meyers KS
      • Mullen LA
      • Ambinder EB.
      Impact of improved screening mammography recall lay letter readability on patient follow-up.
      ). Therefore, as Black patients are more likely to have lower incomes, be uninsured or have public insurance compared to White patients, the overall higher cost of diagnostic mammography poses a substantial obstacle for this patient population especially coupled with the reported barrier of prioritization of other responsibilities for this population (
      • Miller BC
      • Bowers JM
      • Payne JB
      • et al.
      Barriers to mammography screening among racial and ethnic minority women.
      ,
      • Elmore JG
      • Nakano CY
      • Linden HM
      • et al.
      Racial inequities in the timing of breast cancer detection, diagnosis, and initiation of treatment.
      ,
      • Adams SA
      • Smith ER
      • Hardin J
      • et al.
      Racial differences in follow-up of abnormal mammography findings among economically disadvantaged women.
      ). In addition, lack of insurance coverage was associated with lack of optimal diagnostic follow-up for Hispanic patients with a probably benign finding initially detected on screening mammography requiring up to 2 years of diagnostic mammography follow-up evaluation (
      • Lacson R
      • Wang A
      • Cochon L
      • et al.
      Factors associated with optimal follow-up in women with BI-RADS 3 breast findings.
      ).
      Additionally, just as with screening mammography, barriers of transportation to mammography facilities disproportionally affect patients with lower incomes and racial minorities (
      • Syed ST
      • Gerber BS
      • Sharp LK.
      Traveling towards disease: transportation barriers to health care access.
      ,
      • Peipins LA
      • Graham S
      • Young R
      • et al.
      Time and distance barriers to mammography facilities in the Atlanta metropolitan area.
      ,
      • Giuliano A
      • Papenfuss M
      • de Guernsey de Zapien J
      • et al.
      Breast cancer screening among Southwest American Indian women living on-reservation.
      ). Khang et al. in 2017 found that Black patients were more likely to live farther from diagnostic mammography facilities and were less likely to adhere to follow-up recommendations compared to White patients (
      • Khang L
      • Adams SA
      • Steck SE
      • et al.
      Travel distance to screening facilities and completion of abnormal mammographic follow-up among disadvantaged women.
      ). In general, patients who live farther from diagnostic mammography facilities are less likely to adhere to follow-up recommendations compared to patients who live closer (
      • Khang L
      • Adams SA
      • Steck SE
      • et al.
      Travel distance to screening facilities and completion of abnormal mammographic follow-up among disadvantaged women.
      ,
      • Allen JD
      • Shelton RC
      • Harden E
      • et al.
      Follow-up of abnormal screening mammograms among low-income ethnically diverse women: findings from a qualitative study.
      ). Therefore, in the setting of an abnormal screening mammogram, recalled women must endure both direct medical and indirect time costs, which skews against racial minorities with higher incidences of lower SES leading to increased risk of delays in diagnosis.

      DISPARITIES IN BREAST IMAGING RESOURCES – MRI

      Breast MRI is the most sensitive of all breast imaging modalities for the detection and diagnosis of breast cancer (
      • Orel SG
      • Schnall MD.
      MR imaging of the breast for detection, diagnosis and staging of breast cancer.
      ). Incorporation of breast MRI as an adjunct to breast cancer screening in high-risk patients has been shown to not only improve early detection of breast cancer, but also improves overall survival when compared to screening mammography alone (
      • Bae MS
      • Sung JS
      • Bernard-Davila B
      • et al.
      Survival outcomes of screening with breast MRI in women at elevated risk of breast cancer.
      ). However, Haas et al. in 2016 demonstrated that women with a high school education level or lower were reported to be less likely to obtain high-risk screening breast MRI examinations compared to women with a college degree (
      • Haas JS
      • Hill DA
      • Wellman RD
      • et al.
      Disparities in the use of screening magnetic resonance imaging of the breast in community practice by race, ethnicity, and socioeconomic status.
      ). This is also true for average-risk women with less than a college degree. However, there were no significant racial or ethnic differences in the likelihood of obtaining high-risk screening breast MRI. Availability of breast MRI appointments may contribute to this disparity as variability of on-site breast MRI units at breast imaging facilities exist with only about 40% of facilities able to offer breast MRI examinations in communities that serve mostly minority and vulnerable patient populations (
      • Lee CI
      • Bogart A
      • Germino JC
      • et al.
      Availability of advanced breast imaging at screening facilities serving vulnerable populations.
      ). Furthermore, previous studies have shown that geographic access to breast MRI units are worse for Black and American Indian women and women in rural areas. These groups have longer median travel times to these facilities compared to White women (
      • Lee CI
      • Bogart A
      • Germino JC
      • et al.
      Availability of advanced breast imaging at screening facilities serving vulnerable populations.
      ,
      • Onega T
      • Lee CI
      • Benkeser D
      • et al.
      Travel burden to breast MRI and utilization: are risk and sociodemographics related?.
      ,
      • Onega T
      • Hubbard R
      • Hill D
      • et al.
      Geographic access to breast imaging for US women.
      ). Breast MRI is the most expensive modality clinically used for breast cancer screening or diagnostic work-up with average cost of about $1,100 (
      Discuss Your Options
      BREM.
      ). Although no current study has directly evaluated the relationship between cost and access of breast MRI examinations, given the fact that higher education level is overall associated with higher incomes and lower education level populations are less likely to obtain breast MRI examinations, it can be inferred that the deterrent of high cost likely plays a role in preventing access to breast MRI examinations (
      • Onega T
      • Lee CI
      • Benkeser D
      • et al.
      Travel burden to breast MRI and utilization: are risk and sociodemographics related?.
      ,

      U.S Bureau of Labor Statistics. Education pays, 2020. Available at: http://www.bls.gov/careeroutlook/2021/data-on-display/education-pays.htm. Accessed on December 30, 2021.

      ). Furthermore, if cost is a known factor in lower diagnostic mammography follow-up adherence, it is reasonable to expect that this barrier also affects breast MRI, as breast MRI is two to five times more expensive than a diagnostic mammography/ultrasound appointment (
      • Miller BC
      • Bowers JM
      • Payne JB
      • et al.
      Barriers to mammography screening among racial and ethnic minority women.
      ,
      • Elmore JG
      • Nakano CY
      • Linden HM
      • et al.
      Racial inequities in the timing of breast cancer detection, diagnosis, and initiation of treatment.
      ,
      • Adams SA
      • Smith ER
      • Hardin J
      • et al.
      Racial differences in follow-up of abnormal mammography findings among economically disadvantaged women.
      ,
      • Alcusky M
      • Philpotts L
      • Bonafede M
      • et al.
      The patient burden of screening mammography recall.
      ).

      DISPARITIES IN BREAST IMAGING RESOURCES – IMAGE-GUIDED BREAST BIOPSY

      In breast imaging, imaging diagnosis is only half the battle as definitive diagnosis with biopsy is important for surgical and oncologic management of breast cancer. Availability of image-guided biopsy services poses a barrier with stereotactic-guided and MRI-guided biopsy reported as being available only 40% of the time at facilities which serve underserved populations (
      • Lee CI
      • Bogart A
      • Germino JC
      • et al.
      Availability of advanced breast imaging at screening facilities serving vulnerable populations.
      ). In fact, Selove et al. in 2016 found that Black women suffer delays between an abnormal diagnostic mammogram and diagnostic biopsy of up to 60 days and between biopsy and treatment initiation of up to 30 days compared to White women (
      • Selove R
      • Kilbourne B
      • Fadden MK
      • et al.
      Time from screening mammography to biopsy and from biopsy to breast cancer treatment among black and white, women medicare beneficiaries not participating in a health maintenance organization.
      ). This has substantial impact as Black patients are already prone to more advanced breast cancer presentations compared to other races and ethnicities and longer delays of diagnosis and treatment of breast cancer lead to increased mortality (
      • Ooi SL
      • Martinez ME
      • Li CI.
      Disparities in breast cancer characteristics and outcomes by race/ethnicity.
      ,
      • Miller-Kleinhenz JM
      • Collin LJ
      • Seidel R
      • et al.
      Racial disparities in diagnostic delay among women with breast cancer.
      ,
      • Goldman LE
      • Walker R
      • Hubbard R
      • et al.
      Timeliness of abnormal screening and diagnostic mammography follow-up at facilities serving vulnerable women.
      ). As with breast MRI, the cost of image-guided biopsies likely also poses a barrier for disadvantaged patients with costs ranging from hundreds to thousands of dollars depending on the modality and patient insurance status (
      • Alcusky M
      • Philpotts L
      • Bonafede M
      • et al.
      The patient burden of screening mammography recall.
      ,
      • Liberman L
      • Feng TL
      • Dershaw DD
      • et al.
      US-guided core breast biopsy: use and cost-effectiveness.
      ,

      Diagnostic Imaging. Ultrasound-guided breast biopsy gains popularity. Available at: https://www.diagnosticimaging.com/view/ultrasound-guided-breast-biopsy-gains-popularity. Accessed on January 30, 2022.

      ,
      Hologic
      Breast Biopsy.
      ).

      THE IMPACT OF THE COVID-19 PANDEMIC ON BREAST IMAGING DISPARITIES

      Starting in March 2020, significant disruptions in the healthcare workflow in the United States have occurred because of the ongoing COVID-19 pandemic, with breast imaging far from being excluded (
      WHO
      Director-General's opening remarks at the media briefing on COVID-19.
      ). Due to safety concerns, the Society of Breast Imaging (SBI) released recommendations in March 2020 to delay annual screening mammography and diagnostic examinations on patients without clinically concerning symptoms and 6-month follow-up examinations until risk to patient lessened from the pandemic (

      Society of Breast Imaging. Statement on Breast Imaging during the COVID-19 Pandemic. Available at: https://www.sbi-online.org/Portals/0/Position%20Statements/2020/society-of-breast-imaging-statement-on-breast-imaging-during-COVID19-pandemic.pdf. Accessed on December 6, 2021.

      ). Although this delay was short-term as most breast imaging practices began re-opening services in May 2020, the availability for these services upon re-opening was adjusted to accommodate the necessary risk-reduction strategies to mitigate COVID-19 transmission risk to breast imaging patients and staff, including limiting the number of patients in the clinic at a certain time and allowing for social distancing in the waiting rooms (
      Society of Breast Imaging
      SBI Recommendations for a Thoughtful Return to Caring for Patients.
      ). A survey study demonstrated that the COVID-19 pandemic delayed 80% of routine and follow-up breast care appointments, 60% of breast imaging appointments, 67% of reconstruction surgeries, and 30% of breast cancer treatments including lumpectomies and chemotherapy/radiation therapy (
      • Papautsky EL
      • Hamlish T.
      Patient-reported treatment delays in breast cancer care during the COVID-19 pandemic.
      ).
      Projected analysis models predict that the delays in breast cancer diagnosis and treatment during the first 6 months of the pandemic will result in small long-term negative impact on breast cancer mortality by 2030 (
      • Alagoz O
      • Lowry KP
      • Kurian AW
      • et al.
      Impact of the COVID-19 pandemic on breast cancer mortality in the US: estimates from collaborative simulation modeling.
      ). Amornsiripanitch et al. in 2020 demonstrated that racial/ethnic minority and Medicare patients not only had higher rates of screening mammogram cancellations during the COVID-19 pandemic, but also race and insurance status were significant predictors of having an increased relative risk of cancellation (
      • Amornsiripanitch N
      • Chikarmane SA
      • Bay CP
      • et al.
      Patients characteristics related to screening mammography cancellation and rescheduling rates during the COVID-19 pandemic.
      ). This is significant as the COVID-19 pandemic resulted in loss of health insurance for some people due to unemployment and this can amplify cost barriers particularly for underserved patients (
      • Miller BC
      • Bowers JM
      • Payne JB
      • et al.
      Barriers to mammography screening among racial and ethnic minority women.
      ,
      • Elmore JG
      • Nakano CY
      • Linden HM
      • et al.
      Racial inequities in the timing of breast cancer detection, diagnosis, and initiation of treatment.
      ,
      • Adams SA
      • Smith ER
      • Hardin J
      • et al.
      Racial differences in follow-up of abnormal mammography findings among economically disadvantaged women.
      ,
      • Alcusky M
      • Philpotts L
      • Bonafede M
      • et al.
      The patient burden of screening mammography recall.
      ,
      • McIntyre A
      • Brault MW
      • Sommers BD.
      Measuring coverage rates in a pandemic: policy and research challenges.
      ). Furthermore, preliminary data have demonstrated that not all patients are recovering from the initial delays caused by the COVID-19 pandemic equally (
      • Sprague BL
      • Lowry KP
      • Milioretti DL
      • et al.
      Changes in mammography utilization by women's characteristics during the first 5 months of the COVID-19 pandemic.
      ,
      • Lehman CD
      • Mercaldo SF
      • Wang GX
      • et al.
      Screening mammography recovery after COVID-19 pandemic-related closures: associations of facility access and racial and ethnic screening disparities.
      ). Hispanic and Asian patients had lower volumes of rebound screening mammography volumes following resumption of routine breast imaging services compared to patients of other races and ethnicities, resulting in a substantial accumulation of missed mammograms (
      • Sprague BL
      • Lowry KP
      • Milioretti DL
      • et al.
      Changes in mammography utilization by women's characteristics during the first 5 months of the COVID-19 pandemic.
      ). Lehman et al. in 2021 reported that although screening volumes improved for all races after re-opening during May 2020, all races other than White still had disproportionally lower recovery volumes (
      • Lehman CD
      • Mercaldo SF
      • Wang GX
      • et al.
      Screening mammography recovery after COVID-19 pandemic-related closures: associations of facility access and racial and ethnic screening disparities.
      ). Additional patient characteristics such as residing in higher poverty areas, lack of health insurance, need for an interpreter, and longer travel time to breast imaging facilities were associated with a lower likelihood of resuming routine screening mammography following COVID-19 related disruptions (
      • Miller MM
      • Meneveau MO
      • Rochman CM
      • et al.
      Impact of the COVID-19 pandemic on breast cancer screening volumes and patient screening behaviors.
      ).
      Currently there is a paucity of literature on the effects of the COVID-19 pandemic on the workflow and disparities related to other areas of breast imaging such as diagnostic mammography or breast MRI. However, it is reported that the COVID-19 pandemic has resulted in delayed patient presentations of prior early presenting diagnoses before the pandemic in other medical subspecialties which has affected the disease-specific mortality. Gerall et al. in 2021 reports pediatric patients presented later to the emergency department and with more severe symptoms of acute appendicitis during the COVID-19 pandemic peak in Spring of 2020 compared to before the pandemic (
      • Gerall CD
      • DeFazio JR
      • Kahan AM
      • et al.
      Delayed presentation and sub-optimal outcomes of pediatric patients with acute appendicitis during the COVID-19 pandemic.
      ). This led to an increase in the number of complicated acute appendicitis cases on radiologic imaging compared to uncomplicated cases before with worsening patient outcomes (
      • Gerall CD
      • DeFazio JR
      • Kahan AM
      • et al.
      Delayed presentation and sub-optimal outcomes of pediatric patients with acute appendicitis during the COVID-19 pandemic.
      ). Primessnig et al. in 2021 found a significant delay in time from symptom onset to medical contact of ST-elevation myocardial infarction (STEMI) and non-ST-elevation myocardial infarction (NSTEMI) patients during the COVID-19 pandemic peak in Spring of 2020 compared to before which also negatively affected patient mortality (
      • Primessnig U
      • Pieske BM
      • Sherif M.
      Increased mortality and worse cardiac outcome of acute myocardial infarction during the early COVID-19 pandemic.
      ). Therefore, patients with a new palpable lump (the most common presenting symptom of breast cancer) during a COVID-19 pandemic surge theoretically may also have been reluctant to be evaluated, thus delaying the diagnosis of a breast cancer (
      • Mathis KL
      • Hoskin TL
      • Boughey JC
      • et al.
      Palpable presentation of breast cancer persists in the era of screening mammography.
      ). Moving forward, more research is required to investigate if deficiencies exist in other areas of breast imaging outside of screening mammography due to the COVID-19 pandemic.
      Thus, the COVID-19 pandemic has exacerbated the overwhelming disparities which permeate through breast imaging services and highlights the important need to address these barriers to ensure adequate access to breast imaging services for all patients.

      TARGETED INTERVENTIONS TO REDUCE BREAST IMAGING DISPARITY GAPS

      Over the past decade, attempts at alleviating specific factors to improve access and accessibility of breast imaging services to decrease known racial/ethnic and socioeconomic disparities have been made.

      Targeted Interventions – Screening Mammography

      To increase awareness of and adherence to annual screening mammography recommendations, the implementation of patient navigators has been shown to positively impact screening rates among racial minority patient populations; increasing the odds of adherence to almost triple compared to no intervention (
      • Phillips CE
      • Rothstein JD
      • Beaver K
      • et al.
      Patient navigation to increase mammography screening among inner city women.
      ,
      • Gabram SG
      • Lund MJ
      • Gardner J
      • et al.
      Effects of an outreach and internal navigation program on breast cancer diagnosis in an urban cancer center with a large African-American population.
      ,
      • Wells KJ
      • Battaglia TA
      • Dudley DJ
      • et al.
      Patient navigation: state of the art or is it science?.
      ). Patient navigation's effectiveness is derived from the fact that these programs are culturally tailored to the specific patient population they serve with the sole purpose of decreasing cancer health disparities (
      • Mathis KL
      • Hoskin TL
      • Boughey JC
      • et al.
      Palpable presentation of breast cancer persists in the era of screening mammography.
      ). These patient navigators are usually hired based on their experience serving diverse, inner-city patients and have connections and knowledge of existing community programs to better advise and educate their patients (
      • Phillips CE
      • Rothstein JD
      • Beaver K
      • et al.
      Patient navigation to increase mammography screening among inner city women.
      ). Furthermore, most are fluent in languages other than English such as Spanish, which is essential to aiding underserved populations where language barriers could prevent access to health care. Providing education, instructions, and mammography services all in Spanish can significantly increase the adherence to annual screening mammograms in low-income Hispanic populations (
      • Skaer T.L.
      • Robison L.M.
      • Sclar D.A.
      • et al.
      Financial incentive and the use of mammography among Hispanic migrants to the United States.
      ). Patient navigators also facilitate community outreach programs that provide education on the important relationship between the early detection of breast cancer and lower mortality which have proven to be equally as effective at increasing annual screening mammography adherence rates (
      • Gabram SG
      • Lund MJ
      • Gardner J
      • et al.
      Effects of an outreach and internal navigation program on breast cancer diagnosis in an urban cancer center with a large African-American population.
      ).
      In addition to the culturally tailored strategies above using patient navigators, individualized in-person or telephone counseling, individualized letters and reminders, vouchers and coupons for free mammograms, bus passes to allow for transportation to screening mammogram appointments, and bilingual program materials have all been shown to target specific socioeconomic barriers which are common to Black and Hispanic populations to increase annual screening mammography adherence (
      • Legler J
      • Meissner HI
      • Coyne C
      • et al.
      The effectiveness of interventions to promote mammography among women with historically lower rates of screening.
      ,
      • Saywell Jr, RM
      • Champion VL
      • Skinner CS
      • et al.
      A cost-effectiveness comparison of three tailored interventions to increase mammography screening.
      ,
      • Ahmed NU
      • Haber G
      • Semenya KA
      • Hargreaves MK.
      Randomized controlled trial of mammography intervention in insured very low-income women.
      ,
      • Saywell Jr, RM
      • Champion VL
      • Zollinger TW
      • et al.
      The cost effectiveness of 5 interventions to increase mammography adherence in a managed care population.
      ).
      Alternative interventions which appeal to specific cultural activities of communities have also been proven effective to promote annual screening mammography awareness. For instance, radio stations that target Black audiences have been viewed as a trusted source of information for this population, of which a majority report using radio stations specifically programmed with Black audiences in mind to obtain information to make informed life decisions (
      • Leeks KD
      • Hall IJ
      • Johnson-Turbes CA
      • et al.
      Formative development of a culturally appropriate mammography screening campaign for low-income African American women.
      ,
      • Coughlin SS.
      Intervention approaches for addressing breast cancer disparities among African American women.
      ). Hall et al. in 2012 demonstrated that by using Black radio to disseminate information to promote awareness and knowledge about the importance of early detection of breast cancer, this significantly increased women's awareness of breast cancer screening services among Black populations in Georgia (
      • Hall IJ
      • Rim SH
      • Johnson-Turbes CA
      • et al.
      The African American women and mass media campaign: a CDC breast cancer screening project.
      ). Church is reported as one of the most important social institutions in the Black and Hispanic communities and thus, is an ideal setting to offer health care promotion activities for these populations (
      • Markens S
      • Fox SA
      • Taub B
      • et al.
      Role of black churches in health promotion programs: lessons from the Los Angeles mammography promotion in churches program.
      ,
      • Maxwell AE
      • Vargas C
      • Santifer R
      • et al.
      Facilitators and challenges to health promotion in black and latino churches.
      ). Multiple studies have demonstrated that utilizing the church location to provide outreach educational awareness programs or church-based telephone counseling mammography services are just a few examples of how church-related interventions significantly increased annual screening mammography adherence in these populations (
      • Derose KP
      • Fox SA
      • Reigadas E
      • et al.
      Church-based telephone mammography counseling with peer counselors.
      ,
      • Duran N
      • Fox SA
      • Derose KP
      • et al.
      Identifying churches for community-based mammography promotion: lessons from the LAMP study.
      ,
      • Duran N
      • Fox SA
      • Derose KP
      • et al.
      Maintaining mammography adherence through telephone counseling in a church-based trial.
      ,
      • Paskett ED
      • Tatum CM
      • D'Agostino R
      • et al.
      Community-based interventions to improve breast and cervical cancer screening: results of the Forsyth County Cancer Screening (FoCaS) Project.
      ,
      • Agrawal P
      • Chen TA
      • McNeill LH
      • et al.
      Factors associated with breast cancer screening adherence among church-going african american women.
      ).
      Since 2012, the mobile mammography unit (MMU) has been implemented which provides screening mammography services directly to patient neighborhoods as an alternative option to the standard breast imaging facility (
      • Browder C
      • Eberth JM
      • Schooley B
      • et al.
      Mobile mammography: An evaluation of organizational, process, and information systems challenges.
      ). This is a community health resource with no out-of-pocket costs for patients which can help to improve access to health care for women and to encourage these women to receive regular annual screening mammograms (
      • Browder C
      • Eberth JM
      • Schooley B
      • et al.
      Mobile mammography: An evaluation of organizational, process, and information systems challenges.
      ). This is especially important as the common patient demographics that the MMUs serve are Black and Hispanic patients, rural patients, and uninsured patients, all of whom have higher risk of delayed breast cancer diagnosis and breast cancer mortality (
      • Tsapatsaris A
      • Reichman M.
      Project ScanVan: Mobile mammography services to decrease socioeconomic barriers and racial disparities among medically underserved women in NYC.
      ,
      • Stanley E
      • Lewis MC
      • Irshad A
      • et al.
      Effectiveness of a mobile mammography program.
      ). Spak et al. in 2021 demonstrated that the MMU was effective in detecting 14 additional breast cancers in an underserved metropolitan community, all of which were in asymptomatic minority patients (
      • Spak DA
      • Foxhall L
      • Rieber A
      • et al.
      Retrospective review of a mobile mammography screening program in an underserved population within a large metropolitan area.
      ). While MMU offers an opportunity to help bridge screening disparity gaps, its impact is not equal among all minority groups (
      • Roubidoux MA
      • Richards B
      • Honey NE
      • et al.
      Adherence to screening among American Indian women accessing a mobile mammography unit.
      ). Roubidoux et al. in 2021 demonstrated that while the MMU offered American Indian patients the ability to obtain their screening mammograms at a location more geographically accessible, majority of these patients were still not adhering to annual screening despite this intervention to combat geographical barriers (
      • Roubidoux MA
      • Richards B
      • Honey NE
      • et al.
      Adherence to screening among American Indian women accessing a mobile mammography unit.
      ). Overall, the MMU has been an effective outreach strategy for many communities to overcome both racial/ethnic and socioeconomic barriers given the lack of cost to patients and location flexibility to reach both rural patients and other patients with limited access to care (
      • Browder C
      • Eberth JM
      • Schooley B
      • et al.
      Mobile mammography: An evaluation of organizational, process, and information systems challenges.
      ,
      • Tsapatsaris A
      • Reichman M.
      Project ScanVan: Mobile mammography services to decrease socioeconomic barriers and racial disparities among medically underserved women in NYC.
      ,
      • Vang S
      • Margolies LR
      • Jandorf L.
      Mobile mammography participation among medically underserved women: a systematic review.
      ). Continued efforts to improve the ability of MMU to promote annual adherence is still required especially for rural populations such as American Indian and Alaska natives in order to maximize the screening mammography benefits for reducing breasts cancer mortality (
      • Roubidoux MA
      • Richards B
      • Honey NE
      • et al.
      Adherence to screening among American Indian women accessing a mobile mammography unit.
      ).

      Targeted Interventions – Diagnostic Mammography

      To reduce the number of patients lost to follow-up in the setting of an abnormal screening mammogram, targeted communication interventions were implemented with successful results (
      • Nguyen DL
      • Harvey SC
      • Oluyemi E
      • Meyers KS
      • Mullen LA
      • Ambinder EB.
      Impact of improved screening mammography recall lay letter readability on patient follow-up.
      ,
      • Nguyen DL
      • Oluyemi E
      • Meyers KS
      • et al.
      Impact of telephone communication on patient adherence with follow-up recommendations after an abnormal screening mammogram.
      ). Revising the language of the mandated Mammography Quality Standards Act (MQSA) recall lay letter which communicates to patients their abnormal screening mammogram results to FDA recommended readability standards resulted in increased adherence to diagnostic mammography follow-up for all racial/ethnic minority patient populations (
      • Nguyen DL
      • Harvey SC
      • Oluyemi E
      • Meyers KS
      • Mullen LA
      • Ambinder EB.
      Impact of improved screening mammography recall lay letter readability on patient follow-up.
      ). Additionally, implementation of multiple telephone reminder communications in conjunction with this letter also resulted in increased adherence to diagnostic mammography follow-up for all racial/ethnic minority patient populations (
      • Nguyen DL
      • Oluyemi E
      • Meyers KS
      • et al.
      Impact of telephone communication on patient adherence with follow-up recommendations after an abnormal screening mammogram.
      ). Specifically, Nguyen et al. in 2020 demonstrated that improved readability of the recall lay letter significantly improved patient adherence rates of an imaging site whose predominant service population is racial minorities and patients with low SES (
      • Nguyen DL
      • Harvey SC
      • Oluyemi E
      • Meyers KS
      • Mullen LA
      • Ambinder EB.
      Impact of improved screening mammography recall lay letter readability on patient follow-up.
      ). As with annual screening mammogram adherence, implementation of patient navigation programs, especially ones with bilingual services, has also been shown to reduce the number of patients lost to follow-up and delays experienced by racial minority patients between an abnormal screening mammogram and definitive diagnosis (
      • Percac-Lima S
      • Ashburner JM
      • McCarthy AM
      • et al.
      Patient navigation to improve follow-up of abnormal mammograms among disadvantaged women.
      ,
      • Markossian TW
      • Darnell JS
      • Calhoun EA.
      Follow-up and timeliness after an abnormal cancer screening among underserved, urban women in a patient navigation program.
      ,
      • Ramirez AG
      • Pérez-Stable EJ
      • Penedo FJ
      • et al.
      Navigating Latinas with breast screen abnormalities to diagnosis: the six cities study.
      ,
      • Ramirez A
      • Perez-Stable E
      • Penedo F
      • et al.
      Reducing time-to-treatment in underserved Latinas with breast cancer: the Six Cities Study.
      ).
      Furthermore, shortly after the resumption of breast imaging services initially delayed at the beginning of the COVID-19 pandemic, Dontchos et al. in 2021 implemented an immediate-read screening mammography program with the possibility of same-day diagnostic mammography appointments for patients in May 2020 (
      • Dontchos BN
      • Achibiri J
      • Mercaldo SF
      • et al.
      disparities in same-day diagnostic imaging in breast cancer screening: impact of an immediate-read screening mammography program implemented during the COVID-19 pandemic.
      ). Dontchos et al. showed that after implementation, this program significantly decreased racial and ethnic disparities associated with same-day diagnostic imaging in the setting of an abnormal screening mammogram (
      • Dontchos BN
      • Achibiri J
      • Mercaldo SF
      • et al.
      disparities in same-day diagnostic imaging in breast cancer screening: impact of an immediate-read screening mammography program implemented during the COVID-19 pandemic.
      ). Therefore, immediate-read screening mammography programs could be another effective way to decrease the delays in diagnosis experienced by underserved populations.

      Targeted Interventions – Breast Biopsy

      Same-day interventions have also been utilized to reduce disparities related to biopsy appointments as typically breast biopsies may be performed days or even weeks after diagnostic evaluation due to lack of appointment availability, staffing or service availability (
      • Lee CI
      • Bogart A
      • Germino JC
      • et al.
      Availability of advanced breast imaging at screening facilities serving vulnerable populations.
      ,
      • Dontchos BN
      • Narayan AK
      • Seidler M
      • et al.
      Impact of a same-day breast biopsy program on disparities in time to biopsy.
      ). Dontchos et al. in 2019 implemented a same-day biopsy program which resulted in the elimination of all racial/ethnic or insurance-related disparities associated with delays in biopsy appointments prior to implementation (
      • Dontchos BN
      • Narayan AK
      • Seidler M
      • et al.
      Impact of a same-day breast biopsy program on disparities in time to biopsy.
      ).

      FUTURE DIRECTIONS

      There are still multiple known barriers which have not been addressed including high out-of-pocket service costs for breast services other than screening mammography as well as geographical limitations in appointment availability, especially for breast MRI examinations. Furthermore, there are disadvantages of some interventions that need to be addressed to maximize their impact. for example, although both same-day screening programs and MMU have reduced barriers in accessing screening mammography for underserved populations, they do not address the same barriers for the subset of patients who then require diagnostic mammography evaluation (
      • Vang S
      • Margolies LR
      • Jandorf L.
      Mobile mammography participation among medically underserved women: a systematic review.
      ,
      • Dontchos BN
      • Achibiri J
      • Mercaldo SF
      • et al.
      disparities in same-day diagnostic imaging in breast cancer screening: impact of an immediate-read screening mammography program implemented during the COVID-19 pandemic.
      ,
      • Oluyemi E.
      Editorial comment: offering immediate screening mammography interpretation may be an effective way to reduce the racial and ethnic disparity gap in the time to diagnostic follow-up.
      ,
      • Peek ME
      • Han JH.
      Compliance and self-reported barriers to follow-up of abnormal screening mammograms among women utilizing a county mobile mammography van.
      ). In fact, it has been recommended that for either of these interventions to be effective, adequate logistical protocols need to be established to ensure the opportunity for same-day diagnostic evaluation or the capability of tracking patients who require follow-up to ensure that these patients are not lost to follow-up (
      • Oluyemi E.
      Editorial comment: offering immediate screening mammography interpretation may be an effective way to reduce the racial and ethnic disparity gap in the time to diagnostic follow-up.
      ,
      • Peek ME
      • Han JH.
      Compliance and self-reported barriers to follow-up of abnormal screening mammograms among women utilizing a county mobile mammography van.
      ).
      Moving forward, specific areas for improvement include creation of institutional programs to help reduce of out-of-pocket costs for underserved and low SES populations for all breast imaging services, outreach to large philanthropic foundations to sponsor vouchers to help alleviate diagnostic and biopsy costs just like with screening mammography in uninsured patients, increasing the availability of diagnostic services provided with the goal of reducing delays in the time to diagnostic evaluation and biopsies, and increasing the availability of breast MRI appointments in facilities serving predominantly racial/ethnic minority and rural populations.
      Therefore, the crusade for achieving optimal and equal access of care for all populations is far from complete. It is important to continue innovating and improving the interventions that are currently in place especially as we progress through the COVID-19 pandemic where at-risk populations are shown to be disproportionally affected negatively impacting their breast cancer mortality risk.

      Conclusion

      The interventions which have the greatest impact on healthcare disparities address the structural and logistical aspects of breast imaging services as well as the cultural and interpersonal factors which appeal specifically to these communities promoting consistent adherence. Tackling these disparities by addressing the root causes of disadvantaged patients’ psychological barriers (through direct personal communication from telephone protocols to patient navigators) and logistical barriers (from vouchers and mobile mammography units to same-day screening and biopsy programs) demonstrates the persistent attempts of our healthcare system to make progressive strides at closing disparities gap. However, based on the findings discussed in this review, more targeted interventions aimed at ensuring access to all breast imaging services in underserved and low SES populations are still needed. Development and implementation of suggested interventions can help to chip away at the disparity iceberg which separates these underserved populations from the equitable access to health care services that they deserve. Tackling the root cause factors of the ever-widening breast cancer-related disparity gap is critical to meeting the needs of patient populations that are underserved and can lead to continual improvement in the quality of individualized care for patients who have higher breast cancer morbidity and mortality risks.

      Funding

      Eniola Oluyemi reports receiving research funding ( AUR GE Radiology Research Academic Fellowship Award ).

      References

      1. American Cancer Society. How common is breast cancer? Available at: https://www.cancer.org/cancer/breast-cancer/about/how-common-is-breast-cancer.html. Accessed on December 6, 2021.

        • DeSantis CE
        • Fedewa SA
        • Goding Sauer A
        • et al.
        Breast cancer statistics, 2015: convergence of incidence rates between Black and White women.
        CA Cancer J Clin. 2016; 66 (Jan-Feb): 31-42
        • Li CI.
        Racial and ethnic disparities in breast cancer stage, treatment and survival in the United States.
        Ethn Dis. 2005; 15 (2 Suppl 2): S5-S9
        • Vernon SW
        • Tilley BC
        • Neale AV
        • et al.
        Ethnicity, survival, and delay in seeking treatment for symptoms of breast cancer.
        Cancer. 1985; 55: 1563-1571
        • Noone AM
        • Howlader N
        • Krapcho M
        • et al.
        Table 4.18. Cancer of the female breast (invasive): Age-adjusted rates and trends by race/ethnicity, 2011-2015.
        SEER Cancer Stat Rev. 2021; 1975-2015 (Available at: http://seer.cancer.gov/csr/1975_2015/. Accessed on December 6)
        • Ooi SL
        • Martinez ME
        • Li CI.
        Disparities in breast cancer characteristics and outcomes by race/ethnicity.
        Breast Cancer Res Treat. 2011; 127: 729-738
        • Freeman HP
        • Chu KC.
        Determinants of cancer disparities: barriers to cancer screening, diagnosis, and treatment.
        Surg Oncol Clin N Am. 2005; 14: 655-669
        • Perez-Stable EJ
        • Afable-Munsuz A.
        • Kaplan CP
        • et al.
        Factors influencing time to diagnosis after abnormal mammography in diverse women.
        J Women's Health. 2013; 22: 159-166
        • Jones BA
        • Daily A
        • Calvocoressi L
        • et al.
        Inadequate follow-up of abnormal screening mammograms: findings from the race differences in screening mammography process study (United States).
        Cancer Causes Control. 2005; 16: 809-821
        • Syed ST
        • Gerber BS
        • Sharp LK.
        Traveling towards disease: transportation barriers to health care access.
        J Community Health. 2013; 38: 976-993
        • Amornsiripanitch N
        • Ameri SM
        • Goldberg RJ.
        Impact of age, race, and socioeconomic status on women's perceptions and preferences regarding communication of estimated breast cancer risk.
        Acad Radiol. 2021; 28: 655-663
        • Lee CI
        • Bogart A
        • Germino JC
        • et al.
        Availability of advanced breast imaging at screening facilities serving vulnerable populations.
        J Med Screen. 2016; 23 (3): 24-30
        • Groeneveld PW
        • Laufer SB
        • Garber AM.
        Technology diffusion, hospital variation, and racial disparities among elderly Medicare beneficiaries: 1989–2000.
        Med Care. 2005; 43 (4): 320-329
        • Onega T
        • Duell EJ
        • Shi X
        • et al.
        Race versus place of service in mortality among medicare beneficiaries with cancer.
        Cancer. 2010; 116 (6 1): 2698-2706
        • Berg WA.
        Tailored supplemental screening for breast cancer: what now and what next?.
        AJR Am J Roentgenol. 2009; 192 (2): 390-399
      2. Society of Breast Imaging. Statement on Breast Imaging during the COVID-19 Pandemic. Available at: https://www.sbi-online.org/Portals/0/Position%20Statements/2020/society-of-breast-imaging-statement-on-breast-imaging-during-COVID19-pandemic.pdf. Accessed on December 6, 2021.

        • Papautsky EL
        • Hamlish T.
        Patient-reported treatment delays in breast cancer care during the COVID-19 pandemic.
        Breast Cancer Res Treat. 2020; 184: 249-254
        • Alagoz O
        • Lowry KP
        • Kurian AW
        • et al.
        Impact of the COVID-19 pandemic on breast cancer mortality in the US: estimates from collaborative simulation modeling.
        J Natl Cancer Inst. 2021; 113: 1484-1494
        • Sprague BL
        • Lowry KP
        • Milioretti DL
        • et al.
        Changes in mammography utilization by women's characteristics during the first 5 months of the COVID-19 pandemic.
        J Natl Cancer Inst. 2021; 113: 1161-1167
        • Miller MM
        • Meneveau MO
        • Rochman CM
        • et al.
        Impact of the COVID-19 pandemic on breast cancer screening volumes and patient screening behaviors.
        Breast Cancer Res Treat. 2021; 189: 237-246
        • Duffy SW
        • Tabar L
        • AMF Y
        • et al.
        Beneficial effects of consecutive screening mammography examination on mortality from breast cancer: a prospective study.
        Radiology. 2021; 299: 514-547
        • Nguyen DL
        • Harvey SC
        • Oluyemi E
        • Meyers KS
        • Mullen LA
        • Ambinder EB.
        Impact of improved screening mammography recall lay letter readability on patient follow-up.
        J Am Coll Radiol. 2020; 17: 1429-1436
      3. Medicare Mammograms. Available at: medicare.gov/coverage/mammograms. Accessed December 29, 2021.

      4. Kaiser Family Foundation. Coverage of Breast Cancer Screening and Prevention Services. Available at: https://www.kff.org/womens-health-policy/fact-sheet/coverage-of-breast-cancer-screening-and-prevention-services/. Accessed December 29, 2021.

        • Ahmed AT
        • Welch BT
        • Brinjikji W
        • et al.
        Racial disparities in screening mammography in the united states: a systematic review and meta-analysis.
        J Am Coll Radiol. 2017; 14: 157-165
        • Advani P
        • Advani S
        • Nayak P
        • et al.
        Racial/ethnic disparities in use of surveillance mammogram among breast cancer survivors: a systematic review.
        J Cancer Surviv. 2022; 16: 514-530
        • Field TS
        • Doubeni C
        • Fox MP
        • et al.
        Under utilization of surveillance mammography among older breast cancer survivors.
        J Gen Intern Med. 2008; 23: 158-163
        • Miller BC
        • Bowers JM
        • Payne JB
        • et al.
        Barriers to mammography screening among racial and ethnic minority women.
        Soc Sci Med. 2019; 239112494
        • Islam N
        • Patel S
        • Brooks-Griffin Q
        • et al.
        Understanding barriers and facilitators to breast and cervical cancer screening among Muslim women in NEW YORK city: perspective from key informants.
        SM J Community Med. 2017; 3: 1022
        • Azhar S
        • Wyatt LC
        • Jokhakar V
        • et al.
        Associations between spiritual health locus of control, perceived discrimination and breast and cervical cancer screening for muslim american women in New York city.
        Clin Breast Cancer. 2022; 22: e586-e596
        • Peipins LA
        • Graham S
        • Young R
        • et al.
        Time and distance barriers to mammography facilities in the Atlanta metropolitan area.
        J Community Health. 2011; 36: 675-683
        • Giuliano A
        • Papenfuss M
        • de Guernsey de Zapien J
        • et al.
        Breast cancer screening among Southwest American Indian women living on-reservation.
        Prev Med. 1998; 27: 135-143
        • Roubidoux MA
        • Kaur JS
        • Rhoades DA.
        Health disparities in cancer among American Indians and Alaska natives.
        Acad Radiol. 2022; 29: 1013-1021
        • De Munck L
        • de Bock GH
        • Otter R
        • et al.
        Digital vs screen-film mammography in population-based breast cancer screening: performance indicators and tumour characteristics of screen-detected and interval cancers.
        Br J Cancer. 2016; 115: 517-524
        • Sharpe RE
        • Venkataraman S
        • Phillips J
        • et al.
        Increased cancer detection rate and variations in the recall rate resulting from implementation of 3D digital breast tomosynthesis into a population-based screening program.
        Radiology. 2016; 278: 698-706
        • Falomo E
        • Myers K
        • Reichel KF
        • et al.
        Impact of insurance coverage and socioeconomic factors on screening mammography patients’ selection of digital breast tomosynthesis versus full-field digital mammography.
        Breast J. 2018; 24: 1091-1093
        • Lee CI
        • Zhu W
        • Onega T
        • et al.
        Comparative access to and use of digital breast tomosynthesis screening by women's race/ethnicity and socioeconomic status.
        JAMA Netw Open. 2021; 4e2037546
        • Thigpen D
        • Kappler A
        • Brem R.
        The role of ultrasound in screening dense breasts-a review of the literature and practical solutions for implementation.
        Diagnostics (Basel). 2018; 8: 20
        • Discuss Your Options
        BREM.
        2021 (Available at: http://www.bremfoundation.org/screening-options. Accessed December 29)
        • Ezratty C
        • Vang S
        • Brown J
        • et al.
        Racial/ethnic differences in supplemental imaging for breast cancer screening in women with dense breasts.
        Breast Cancer Res Treat. 2020; 182: 181-185
        • Miller-Kleinhenz JM
        • Collin LJ
        • Seidel R
        • et al.
        Racial disparities in diagnostic delay among women with breast cancer.
        J Am Coll Radiol. 2021; 18 (Oct): 1384-1393
        • Goldman LE
        • Walker R
        • Hubbard R
        • et al.
        Timeliness of abnormal screening and diagnostic mammography follow-up at facilities serving vulnerable women.
        Med Care. 2013; 51: 307-314
        • Ramirez AG
        • Pérez-Stable EJ
        • Talavera GA
        • et al.
        Time to definitive diagnosis of breast cancer in Latina and non-Hispanic White women: the six cities study.
        Springerplus. 2013; 2: 84
        • Nguyen KH
        • Pasick RJ
        • Stewart SL
        • et al.
        Disparities in abnormal mammogram follow-up time for Asian women compared with non-Hispanic White women and between Asian ethnic groups.
        Cancer. 2017; 123: 3468-3475
        • Press R
        • Carrasquillo O
        • Sciacca RR
        • et al.
        Racial/ethnic disparities in time to follow-up after an abnormal mammogram.
        J Womens Health (Larchmt). 2008; 17: 923-930
        • Gorin SS
        • Heck JE
        • Cheng B
        • et al.
        Delays in breast cancer diagnosis and treatment by racial/ethnic group.
        Arch Intern Med. 2006; 166: 2244-2252
        • Elmore JG
        • Nakano CY
        • Linden HM
        • et al.
        Racial inequities in the timing of breast cancer detection, diagnosis, and initiation of treatment.
        Med Care. 2005; 43: 141-148
        • Adams SA
        • Smith ER
        • Hardin J
        • et al.
        Racial differences in follow-up of abnormal mammography findings among economically disadvantaged women.
        Cancer. 2009; 115: 5788-5797
        • Lacson R
        • Wang A
        • Cochon L
        • et al.
        Factors associated with optimal follow-up in women with BI-RADS 3 breast findings.
        J Am Coll Radiol. 2020; 17: 469-474
        • Khang L
        • Adams SA
        • Steck SE
        • et al.
        Travel distance to screening facilities and completion of abnormal mammographic follow-up among disadvantaged women.
        Ann Epidemiol. 2017; 27: 35-41
        • Allen JD
        • Shelton RC
        • Harden E
        • et al.
        Follow-up of abnormal screening mammograms among low-income ethnically diverse women: findings from a qualitative study.
        Patient Educ Couns. 2008; 72: 283-292
        • Orel SG
        • Schnall MD.
        MR imaging of the breast for detection, diagnosis and staging of breast cancer.
        Radiology. 2001; 220: 13-30
        • Bae MS
        • Sung JS
        • Bernard-Davila B
        • et al.
        Survival outcomes of screening with breast MRI in women at elevated risk of breast cancer.
        J Breast Imaging. 2020; 2: 29-35
        • Haas JS
        • Hill DA
        • Wellman RD
        • et al.
        Disparities in the use of screening magnetic resonance imaging of the breast in community practice by race, ethnicity, and socioeconomic status.
        Cancer. 2016; 122: 611-617
        • Onega T
        • Lee CI
        • Benkeser D
        • et al.
        Travel burden to breast MRI and utilization: are risk and sociodemographics related?.
        J Am Coll Radiol. 2016; 13: 611-619
        • Onega T
        • Hubbard R
        • Hill D
        • et al.
        Geographic access to breast imaging for US women.
        J Am Coll Radiol. 2014; 11: 874-882
      5. U.S Bureau of Labor Statistics. Education pays, 2020. Available at: http://www.bls.gov/careeroutlook/2021/data-on-display/education-pays.htm. Accessed on December 30, 2021.

        • Alcusky M
        • Philpotts L
        • Bonafede M
        • et al.
        The patient burden of screening mammography recall.
        J Womens Health (Larchmt). 2014; (23 Suppl 1): S11-S19
        • Selove R
        • Kilbourne B
        • Fadden MK
        • et al.
        Time from screening mammography to biopsy and from biopsy to breast cancer treatment among black and white, women medicare beneficiaries not participating in a health maintenance organization.
        Womens Health Issues. 2016; 26: 642-647
        • Liberman L
        • Feng TL
        • Dershaw DD
        • et al.
        US-guided core breast biopsy: use and cost-effectiveness.
        Radiology. 1998; 208 (Sep): 717-723
      6. Diagnostic Imaging. Ultrasound-guided breast biopsy gains popularity. Available at: https://www.diagnosticimaging.com/view/ultrasound-guided-breast-biopsy-gains-popularity. Accessed on January 30, 2022.

        • Hologic
        Breast Biopsy.
        2022 (Available at: https://www.hologic.com/sites/default/files/2022/MISC-03035_Rev_010_Breast_Biopsy_Coding_Guide_2022.pdf?fbclid=IwAR0kW7n-tEIYjDf1QrSUn6_AlLhdv7oK79bQhAAafCRZEs-VabXaf8Ae-6E. Accessed on January 30)
        • WHO
        Director-General's opening remarks at the media briefing on COVID-19.
        World Health Organization (WHO), 2020 (11 MarchAvailable at: https://www.who.int/dg/speeches/detail/who-director-general-s-opening-remarks-at-the-media-briefing-on-covid-19—11-march-2020. Accessed December 30, 2021)
        • Society of Breast Imaging
        SBI Recommendations for a Thoughtful Return to Caring for Patients.
        2021 (Available at: https://www.sbi-online.org/Portals/0/Position%20Statements/2020/SBI-recommendations-for-a-thoughtful-return-to-caring-for-patients_May-5-2020.pdf. Accessed on December 30)
        • Amornsiripanitch N
        • Chikarmane SA
        • Bay CP
        • et al.
        Patients characteristics related to screening mammography cancellation and rescheduling rates during the COVID-19 pandemic.
        Clin Imaging. 2021; 80: 205-210
        • McIntyre A
        • Brault MW
        • Sommers BD.
        Measuring coverage rates in a pandemic: policy and research challenges.
        JAMA Health Forum. 2020; 1e201278
        • Lehman CD
        • Mercaldo SF
        • Wang GX
        • et al.
        Screening mammography recovery after COVID-19 pandemic-related closures: associations of facility access and racial and ethnic screening disparities.
        AJR. 2022; 218: 988-996
        • Gerall CD
        • DeFazio JR
        • Kahan AM
        • et al.
        Delayed presentation and sub-optimal outcomes of pediatric patients with acute appendicitis during the COVID-19 pandemic.
        J Pediatr Surg. 2021; 56: 905-910
        • Primessnig U
        • Pieske BM
        • Sherif M.
        Increased mortality and worse cardiac outcome of acute myocardial infarction during the early COVID-19 pandemic.
        ESC Heart Fail. 2021; 8: 333-343
        • Mathis KL
        • Hoskin TL
        • Boughey JC
        • et al.
        Palpable presentation of breast cancer persists in the era of screening mammography.
        J Am Coll Surg. 2010; 210 (Mar): 314-318
        • Phillips CE
        • Rothstein JD
        • Beaver K
        • et al.
        Patient navigation to increase mammography screening among inner city women.
        J Gen Intern Med. 2011; 26: 123-129
        • Gabram SG
        • Lund MJ
        • Gardner J
        • et al.
        Effects of an outreach and internal navigation program on breast cancer diagnosis in an urban cancer center with a large African-American population.
        Cancer. 2008; 113: 602-607
        • Wells KJ
        • Battaglia TA
        • Dudley DJ
        • et al.
        Patient navigation: state of the art or is it science?.
        Cancer. 2008; 113: 1999-2010
        • Skaer T.L.
        • Robison L.M.
        • Sclar D.A.
        • et al.
        Financial incentive and the use of mammography among Hispanic migrants to the United States.
        Health Care Women Int. 1996; 17: 281-291
        • Legler J
        • Meissner HI
        • Coyne C
        • et al.
        The effectiveness of interventions to promote mammography among women with historically lower rates of screening.
        Cancer Epidemiol Biomarkers Prev. 2002; 11: 59-71
        • Saywell Jr, RM
        • Champion VL
        • Skinner CS
        • et al.
        A cost-effectiveness comparison of three tailored interventions to increase mammography screening.
        J Womens Health (Larchmt). 2004; 13: 909-918
        • Ahmed NU
        • Haber G
        • Semenya KA
        • Hargreaves MK.
        Randomized controlled trial of mammography intervention in insured very low-income women.
        Cancer Epidemiol Biomarkers Prev. 2010; 19: 1790-1798
        • Saywell Jr, RM
        • Champion VL
        • Zollinger TW
        • et al.
        The cost effectiveness of 5 interventions to increase mammography adherence in a managed care population.
        Am J Manag Care. 2003; 9: 33-44
        • Leeks KD
        • Hall IJ
        • Johnson-Turbes CA
        • et al.
        Formative development of a culturally appropriate mammography screening campaign for low-income African American women.
        J Health Disparit Res Pract. 2012; 5: 42-61
        • Coughlin SS.
        Intervention approaches for addressing breast cancer disparities among African American women.
        Ann Transl Med Epidemiol. 2014; 1: 1001
        • Hall IJ
        • Rim SH
        • Johnson-Turbes CA
        • et al.
        The African American women and mass media campaign: a CDC breast cancer screening project.
        J Womens Health (Larchmt). 2012; 21: 1107-1113
        • Markens S
        • Fox SA
        • Taub B
        • et al.
        Role of black churches in health promotion programs: lessons from the Los Angeles mammography promotion in churches program.
        Am J Public Health. 2002; 92: 805-810
        • Maxwell AE
        • Vargas C
        • Santifer R
        • et al.
        Facilitators and challenges to health promotion in black and latino churches.
        J Racial Ethn Health Disparities. 2022; 9: 59-67
        • Derose KP
        • Fox SA
        • Reigadas E
        • et al.
        Church-based telephone mammography counseling with peer counselors.
        J Health Commun. 2000; 5: 175-188
        • Duran N
        • Fox SA
        • Derose KP
        • et al.
        Identifying churches for community-based mammography promotion: lessons from the LAMP study.
        Health Educ Behav. 2005; 32: 536-548
        • Duran N
        • Fox SA
        • Derose KP
        • et al.
        Maintaining mammography adherence through telephone counseling in a church-based trial.
        Am J Public Health. 2000; 90: 1468-1471
        • Paskett ED
        • Tatum CM
        • D'Agostino R
        • et al.
        Community-based interventions to improve breast and cervical cancer screening: results of the Forsyth County Cancer Screening (FoCaS) Project.
        Cancer Epidemiol Biomarkers Prevent. 1999; 8: 453-459
        • Agrawal P
        • Chen TA
        • McNeill LH
        • et al.
        Factors associated with breast cancer screening adherence among church-going african american women.
        Int J Environ Res Public Health. 2021; 18: 8494
        • Browder C
        • Eberth JM
        • Schooley B
        • et al.
        Mobile mammography: An evaluation of organizational, process, and information systems challenges.
        Healthc (Amst). 2015; 3: 49-55
        • Tsapatsaris A
        • Reichman M.
        Project ScanVan: Mobile mammography services to decrease socioeconomic barriers and racial disparities among medically underserved women in NYC.
        Clin Imaging. 2021; 78: 60-63
        • Stanley E
        • Lewis MC
        • Irshad A
        • et al.
        Effectiveness of a mobile mammography program.
        AJR. 2017; 209: 1426-1429
        • Spak DA
        • Foxhall L
        • Rieber A
        • et al.
        Retrospective review of a mobile mammography screening program in an underserved population within a large metropolitan area.
        Acad Radiol. 2022; 29 (Suppl 1(Suppl 1)): S173-S179
        • Roubidoux MA
        • Richards B
        • Honey NE
        • et al.
        Adherence to screening among American Indian women accessing a mobile mammography unit.
        Acad Radiol. 2021; 28: 944-949
        • Vang S
        • Margolies LR
        • Jandorf L.
        Mobile mammography participation among medically underserved women: a systematic review.
        Prev Chronic Dis. 2018; 15: E140
        • Nguyen DL
        • Oluyemi E
        • Meyers KS
        • et al.
        Impact of telephone communication on patient adherence with follow-up recommendations after an abnormal screening mammogram.
        J Am Coll Radiol. 2020; 17: 1139-1148
        • Percac-Lima S
        • Ashburner JM
        • McCarthy AM
        • et al.
        Patient navigation to improve follow-up of abnormal mammograms among disadvantaged women.
        J Womens Health (Larchmt). 2015; 24: 138-143
        • Markossian TW
        • Darnell JS
        • Calhoun EA.
        Follow-up and timeliness after an abnormal cancer screening among underserved, urban women in a patient navigation program.
        Cancer Epidemiol Biomarkers Prev. 2012; 21: 1691-1700
        • Ramirez AG
        • Pérez-Stable EJ
        • Penedo FJ
        • et al.
        Navigating Latinas with breast screen abnormalities to diagnosis: the six cities study.
        Cancer. 2013; 119: 1298-1305
        • Ramirez A
        • Perez-Stable E
        • Penedo F
        • et al.
        Reducing time-to-treatment in underserved Latinas with breast cancer: the Six Cities Study.
        Cancer. 2014; 120: 752-760
        • Dontchos BN
        • Achibiri J
        • Mercaldo SF
        • et al.
        disparities in same-day diagnostic imaging in breast cancer screening: impact of an immediate-read screening mammography program implemented during the COVID-19 pandemic.
        AJR. 2022; 218: 270-278
        • Dontchos BN
        • Narayan AK
        • Seidler M
        • et al.
        Impact of a same-day breast biopsy program on disparities in time to biopsy.
        J Am Coll Radiol. 2019; 16: 1554-1560
        • Oluyemi E.
        Editorial comment: offering immediate screening mammography interpretation may be an effective way to reduce the racial and ethnic disparity gap in the time to diagnostic follow-up.
        AJR. 2022; 218: 278
        • Peek ME
        • Han JH.
        Compliance and self-reported barriers to follow-up of abnormal screening mammograms among women utilizing a county mobile mammography van.
        Health Care Women Int. 2009; 30: 857-870