Follow-up after an abnormal screening mammogram: Impact of a pandemic on mobile mammography patients

INTRODUCTION

On January 20, 2020, the United States Centers for Disease Control and Prevention acknowledged the first confirmed case of COVID-19 infection, followed shortly by the World Health Organization’s declaration of a public health emergency of international concern on January 30–31.^[1] Thus began the pandemic. As hospitals became overrun with COVID-19 patients, travel was discouraged or banned, non-essential workers were encouraged to work from home or were laid off, and non-emergent medical procedures and clinic appointments were delayed. Although the World Health Organization and the Centers for Disease Control and Prevention declared the end of the global public health emergency on May 5, 2023, the effects of the pandemic continue to shape our lives today.^[2]

The imaging literature about COVID-19 included findings secondary to infection in the chest and brain and post-vaccination changes in axillary nodes.^[3-6] Aside from this, the pandemic also affected the volume of imaging studies performed. Examinations deemed non-emergent, such as screening mammograms (sMGs), had a sharp decrease— sMG volumes reduced by >50% at many centers.^[7-9] This reduction varied across different demographic groups, with some centers experiencing a complete rebound in patient volumes after the pandemic and others reporting only partial recovery.^[8,10,11] A prior publication from our institution examined the demographics of 238,776 sMG patients from February 1, 2018, through June 20, 2022, documenting shifts in screening volume and patient composition during the pandemic, but did not distinguish between mobile and non-mobile patients and did not evaluate follow-up care after abnormal results.^[11] The present study extends that work by focusing specifically on turnaround time (TAT) from abnormal sMG to diagnostic mammography, a metric with direct implications for timely cancer diagnosis, with particular attention to the mobile mammography population, given its focus on lower-resource communities. Data from other centers have found that those most affected by the pandemic include racial and ethnic minority groups, patients living in urban and rural areas (as opposed to suburban areas), uninsured patients, and patients with lower educational levels.^[10,12-14]

While we know that the COVID-19-related disruptions were associated with decreased cancers detected, one aspect of COVID-19’s effects on breast cancer care that is not as fully studied is follow-up diagnostic mammography after an abnormal sMG.^[15] Timely follow-up after an abnormal sMG is clinically critical, as delays in diagnostic workup have been associated with delayed cancer diagnosis and worse patient outcomes.^[16] One center experienced a persistent decrease in diagnostic mammography volumes post-pandemic, even though their sMG volumes surpassed pre-pandemic levels, demonstrating that different factors may be at play for these patients.^[10] Our study focuses on the TAT between an abnormal sMG and diagnostic mammography, with an emphasis on mobile sMG patients, given that our mobile program focuses on lower-resource communities (as opposed to non-mobile sMG patients who undergo sMG at our brick-and-mortar imaging centers). We hypothesized that TATs for all patients, both mobile and non-mobile, would increase during the pandemic due to reduced imaging capacity and pandemic-related disruptions to care.

MATERIAL AND METHODS

RESULTS

During the pre-pandemic time period, 11,439 patients underwent 14,161 mobile sMG, and 28,737 patients underwent 57,840 non-mobile sMG. During the pandemic time period, 6805 patients underwent 7663 mobile sMG, and 32,655 patients underwent 53,540 non-mobile sMG. After excluding abnormal sMG (breast imaging-reporting and data system assessment category 0) without sufficient follow-up data for analysis, our final study cohorts consisted of data for the following abnormal sMG with sufficient follow-up to calculate TATs: For the pre-pandemic time period, 264 abnormal mobile sMG in patients with insurance, 1675 mobile sMG in patients without insurance, 5674 non-mobile sMG in patients with insurance, and 70 non-mobile sMG in patients without insurance; for the pandemic time period, 7 mobile sMG in patients with insurance, 954 mobile sMG in patients without insurance, 5895 non-mobile sMG in patients with insurance, and 90 non-mobile sMG in patients without insurance [Figure 1].

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Figure 1: Inclusion criteria for this project required patients to have received a screening mammogram and a diagnostic mammogram within the pre-pandemic and pandemic time periods. Patients were also required to have complete demographic data, leading to a final sample size of 14,629 patients.

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Out of the patients screened, 14,719 were recalled from screening and had diagnostic mammograms (2900 mobile mammography patients and 11,819 non-mobile mammography patients). We only analyzed the time between screening and diagnostic mammography because there was an inadequate sample size for statistically significant analysis of time to biopsy. Our sample size of patients who received both screening and diagnostic mammography and had complete demographic data consisted of 14,629 patients [Figure 1].

The demographics of the unique patients in each cohort per time period are shown in Table 1, and some significant differences deserve mention here: Our mobile sMG population is younger than their non-mobile sMG counterparts, while our mobile uninsured cohort is younger, most commonly Hispanic, most commonly of Other race, and of lower income status (all p < 0.001).

There was a significant difference in TATs between mobile insured, mobile uninsured, non-mobile insured, and non-mobile uninsured patients for both time periods [Tables 2 and 3]. We focused on mobile uninsured and non-mobile insured patients since these populations had larger and more comparable sample sizes: median TATs for mobile uninsured patients increased from 41 days during the pre-pandemic period to 51 days during the pandemic period (p < 0.001), while median TATs for non-mobile insured patients decreased from 20 days during the pre-pandemic period to 14 days during the pandemic period (p < 0.001).

Importantly, analysis of the TATs showed a strong right-skew for all groups [Figure 2] with the majority of follow-up studies performed within 100 days after sMG. Due to the right skew, median times were determined to provide a more accurate representation of the times involved. A plot of the median TATs [Figure 3] highlights the statistically significant difference in trends for TAT between mobile uninsured and non-mobile insured patients. The median TAT for mobile uninsured patients was 41 days for the pre-pandemic time period and 51 days for the pandemic time period. The median TAT for non-mobile insured patients was 20 days pre-pandemic and 14 days pandemic. Both differences were statistically significant (P < 0.001). Mobile insured and non-mobile uninsured patients made up a minority of the study group, and the differences seen in these groups did not show a significant difference. Multiple linear regression analysis showed a statistically significant interaction between mobile and the time period (p < 0.001), indicating that the relationship between pandemic period and TAT differed significantly between mobile and non-mobile patients: TATs increased for mobile uninsured patients during the pandemic while decreasing for non-mobile insured patients [Figure 3].

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Figure 2: The turnaround time in days between an abnormal screening mammogram and the subsequently performed diagnostic mammogram was highly right-skewed for all groups (A) mobile uninsured pre-pandemic, (B) non-mobile insured pre-pandemic, (C) mobile uninsured pandemic, and (D) non-mobile insured pandemic, with most patient completing diagnostic mammograms within 100 days.

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Figure 3: Plot of the median turnaround time (TAT) in days between an abnormal screening mammogram and the subsequently performed diagnostic mammogram in the two largest cohorts, mobile uninsured and non-mobile insured, illustrates a statistically significant trend with an increase in the TAT for mobile uninsured patients and decrease in the TAT for non-mobile insured patients.

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On multiple linear regression analysis [Table 3], there was a significant difference in TATs between time periods, mobile mammography (vs. non-mobile mammography), and insurance status. The significant interaction term indicated that after the COVID-19 pandemic, the gap in median TAT from screening to diagnostic mammography between mobile uninsured and non-mobile insured patients increased. After adjusting for pandemic time, mobile, and insurance status, there was a significant increase in TATs for patient-reported African American, Asian, and Other races compared with White race (African American: 27% longer, p < 0.001; Asian: 14% longer, p = 0.004; Other: 14% longer, p = 0.02). Of note, 93% of Hispanic patients used “Other” as their race at our institution.^[11] Age, ethnicity, and income (as estimated by postal code) did not show statistical significance.

DISCUSSION

This work sought to study the effects of the COVID-19 pandemic on the TAT between an abnormal sMG and diagnostic mammography for two diverse groups of patients: Those receiving their screening examinations through our mobile mammography program and those receiving theirs at our brick-and-mortar imaging centers. The pandemic was associated with a significant divergence in TATs between these two groups, with mobile uninsured patients experiencing longer delays and non-mobile insured patients experiencing shorter ones (p < 0.001 for both). Increased TATs were associated with Asian, African American, and Other race compared with White race (Asian, p =0.004; African American, p < 0.001; and Other, p = 0.02) and self-pay insurance status (p = 0.006). These race-based findings should be interpreted with caution, given the self-reported nature of race data and the fact that 93% of Hispanic patients at our institution selected “Other” as their race category.^[11]

Published benchmarks for the time from an abnormal sMG to diagnostic follow-up vary, but typically fall within 2–4 weeks. For example, the average wait in one U.S. study was about 21 days (range 17–25 days), as reported by mean.^[15] National quality measures have also cited TATs as short as approximately 6–7 working days in some high-performing centers.^[15] However, studies evaluating COVID-19’s effect on TATs are limited with the exception of prior reports describing accelerated diagnostic pathways intended to minimize return visits for patients. For example, a European radiology group found that the diagnostic interval (from diagnostic mammogram to final diagnosis) dropped from a median of 15 days pre-pandemic to just 1 day during the first COVID-19 wave, with 50% of patients completing assessment on the initial visit.^[18] This study also reported that 90^th percentile times shortened from approximately 63–21 days. These reports suggest that COVID-related service reengineering, such as rapid diagnostic units and single-visit workups, enabled significantly shorter TATs than pre-COVID benchmarks. Our mobile sMG program might benefit from similar service re-engineering approaches.

Our hypothesis that TATs would increase for all patients during and after the COVID-19 pandemic was incorrect, so we further investigated our clinic operation pathways to see what, if any, changes were made to account for these TAT differences.

In 2019, the nurse navigator position was introduced to the breast radiology clinic. These nurse navigators communicate with referring clinicians and patients for all patients whose sMG was assigned a BI-RADS category 0. They contact referring providers external to our institution by phone within 24 h of an abnormal finding report, providing results, education, and assistance with coordination of care, including follow-up imaging and procedures. They contact our institution’s referring providers through either secure email or messaging within our electronic medical record. If a patient does not have a local provider, the nurse navigators assist with referral to a primary clinical team within our institution (with oversight from that team’s primary nurse navigator for care coordination).

Our mobile mammography program has coordinators who communicate with each patient’s referring provider, who is external to our institution. These coordinators often are forced to rely on the external clinics and providers to send reminders for patient appointments and follow-up. Abnormal sMG results are communicated by letter to the patient and the referring clinician.^[19] Clinicians are contacted through secure email. Patients are initially notified with a lay results letter sent through the United States Postal Service mail, and then a certified letter if no response is received. Since the mobile mammography program only offers sMG, referrals for diagnostic mammograms and biopsies for uninsured patients are sent to one of the main institution’s satellite clinics or one of a few partnered community breast imaging centers unaffiliated with our institution.

This study found a divergence in TATs between mobile uninsured and non-mobile insured patients, a difference that widened during the pandemic. While a prior publication from our institution characterized demographic shifts in the screening population during the pandemic^[11] that work did not evaluate follow-up after abnormal results or distinguish between mobile and non-mobile patients. To the best of our knowledge, the present study is the first to examine pandemic-related TAT differences stratified by mobile mammography status, aside from the single-visit work-up studies mentioned above. This is especially important as a delay in follow-up imaging has implications for breast cancer diagnosis and mortality. Some studies have suggested that COVID-19 resulted in delayed cancer diagnosis and higher stage of cancer at diagnosis, and increased TAT may be a contributing factor.^[20,21]

Our work has identified a potential target for future quality improvement projects to further investigate and improve TATs for mobile patients with abnormal sMGs. Given that mobile coordinators currently rely on external providers to facilitate follow-up and that results are communicated by postal mail, several targeted strategies warrant consideration. First, embedding dedicated patient navigators within the mobile program, rather than relying solely on institutional navigators who serve non-mobile patients, could improve direct outreach and appointment coordination for this population.^[22] Second, centralized scheduling for diagnostic mammography at the time of an abnormal sMG result, rather than routing referrals through external clinics, could reduce delays attributable to fragmented communication pathways.^[23] Third, where logistically feasible, same-day or rapid diagnostic protocols, as have been implemented in other settings, may shorten TATs for mobile patients who face transportation and scheduling barriers.^[18] In addition, surveying patients directly would provide further insight into individual-level barriers to follow-up care that these structural interventions may not fully address.^[24]

These findings have broader programmatic and policy implications for mobile mammography services. Mobile programs that serve uninsured and underinsured populations are often funded and evaluated primarily on screening volume, with less attention paid to the downstream diagnostic pathway. Our data suggest that funding models and program metrics should extend beyond screening to encompass follow-up care, including navigation support, diagnostic imaging access, and referral coordination. At the programmatic level, mobile mammography services may benefit from formal partnerships with community diagnostic centers to streamline referral pathways and reduce dependence on external providers for appointment reminders and follow-up. At a broader policy level, these findings underscore the importance of evaluating mobile programs not only by their reach but by their ability to ensure equitable and timely access to the full continuum of breast cancer care.

This study had several limitations. First, its retrospective single-institution design limits generalizability, as the structure of our mobile program, including Project VALET funding, external referring providers, and a 2-h travel radius, may not be representative of mobile mammography programs at other institutions. Second, race and ethnicity data were self-reported and subject to misclassification. As noted, 93% of Hispanic patients at our institution selected “Other” as their race category,^[11] meaning that race-based TAT findings, particularly for the “Other” group, should be interpreted with this classification overlap in mind. Third, biopsy-level outcomes could not be analyzed due to inadequate sample size at that stage of the care continuum, limiting our ability to assess the downstream clinical impact of TAT delays. Fourth, individual income was not directly measured; estimates were derived from the postal code, which is a proxy that may not accurately reflect individual socioeconomic status. Finally, our mobile sMG program was paused from March 7 to July 7, 2020, so the acute phase of the pandemic is not captured in the mobile patient data, which may have resulted in an underestimate of the full pandemic impact on TATs for this population.

CONCLUSION

The COVID-19 pandemic widened pre-existing disparities in follow-up care after an abnormal sMG, with mobile uninsured patients experiencing longer delays while non-mobile insured patients saw improved TATs. These findings underscore the need for targeted interventions, such as enhanced navigation, improved communication with external clinics, and streamlined diagnostic pathways, to support mobile uninsured patients who face structural barriers to timely follow-up care. Addressing these inequities is essential to ensuring timely cancer diagnoses and equitable access to care across all patient groups.