key: cord-0852884-snqeb24s
authors: Heller, Samantha L.
title: Impact of the Pandemic on Breast Cancer Diagnoses
date: 2021-10-19
journal: Radiology
DOI: 10.1148/radiol.2021212477
sha: c33ff5930cb8bc3068146c491c4a390683a917ce
doc_id: 852884
cord_uid: snqeb24s

nan

At the height of the COVID-19 pandemic in the spring of 2020, many breast imaging practices purposefully halted mammographic screening to minimize patient and staff exposure to the virus. Multidisciplinary professional societies formally issued guidelines advancing this approach. On March 26, 2020, for example, the American College of Radiology and the American Society of Breast Surgeons issued a joint statement recommending that "medical facilities postpone all breast screening exams (screening mammography, ultrasound, and MRI) effective immediately" (1) . The COVID-19 Pandemic Breast Cancer Consortium categorized breast imaging into priority levels, defining mammographic breast cancer screening for average-risk patients as a low priority examination that could be delayed until the postpandemic period (2) . Diagnostic imaging for suspicious symptoms or abnormal mammograms was considered to be of higher, albeit non-urgent, priority. In most practices, a return to standard breast cancer imaging recommendations was instituted in the summer of 2020 (3).

The effects of the pandemic disruptions remain largely unknown, but are of great interest due to their potential longer-term implications for patient prognosis and mortality.

In this issue of Radiology, Lowry and colleagues (4) assess the short-term effects of the pandemic on screening and diagnostic breast imaging cancer detection and biopsy recommendations. They analyzed Breast Cancer Surveillance Consortium (BCSC) data from 7 breast imaging registries (66 facilities), comparing breast biopsy recommendations and breast cancers diagnosed before and during the pandemic with respect to the method of detection (screen-detected vs symptomatic cancers) and patient level characteristics. The authors found that biopsies decreased precipitously in April 2020 compared to April 2019 (76% decrease, 236 I n p r e s s biopsies recommended in 2020 versus 1000 in 2019). Overall, 24% fewer cancers (1,650 in 2020 versus 2,171 in 2019; p<0.001) were detected from March to September 2020 as compared to 2019. These differences were attributable predominantly to a decrease in the number of screen-detected, rather than symptomatic, cancers. Specifically, there was a significant 38% drop in cumulative screen-detected cancers identified in 2020 (722 cancers)

compared to the 1169 screen-detected cancers found in 2019 (p < .001). In comparison, there was no significant difference in cumulative symptomatic cancer detection before and during the pandemic, with 965 symptomatic cancers reported in 2019 and 895 in 2020 (p = .27). In addition, the authors found that the decrease in cancer diagnoses was greatest in Asian women (53% decline), followed by Hispanic women (43% decline) and then Black women (27% decline).

This study is, to our knowledge, the first observational (non-modeling) work to assess the effects of the pandemic on U.S. imaging-based breast cancer diagnosis directly. It expands prior literature, including an earlier BCSC paper, which assessed pandemic effects on mammographic utilization and suggested the possibility of longer-term screening deficits (5) . The findings are also in accord with a recent Dutch study by Eijkelboom and colleagues, who reported a drop in cancer detection during the pandemic, and specifically a decrease in the number of screendetected rather than symptomatic cancers (6) . In the Dutch program, screen-detected cancers 

The key impact of the pandemic in terms of the effects on breast cancer diagnoses may therefore emerge from a delay in screening exams rather than from a delay in imaging work-up of symptomatic cases. What are the theoretical consequences of screening deficits? Screening mammography works by detecting small, invasive node-negative cancers before they metastasize. In multiple observational and randomized controlled trials, mammographic screening has been proven to decrease mortality, and women who are screened have been shown to have better outcomes than those who are not screened (7) . In addition, women undergoing annual screening exams exhibit significantly higher detection rates of smaller, better prognosis cancers compared to women who undergo biennial screening, perhaps particularly true for premenopausal women (8, 9) . It follows that the toll of the pandemic on cancer stage at detection and patient prognosis has the potential to be more marked for those women who do not return for their screening exam in the immediate post-pandemic period, but instead wait until the following year-or even longer-to resume their imaging. This begs the question as to whether the majority of the women at the national level who missed their screening exams will return for their imaging with only a short delay, or instead will forgo screening until a longer interval has passed. The fact that the screening shortfall was still not compensated for at the end of the BCSC study period (4) suggests that pandemic-based screening deficits may well be longer-term in nature, although it would be important to review at least a full year's worth of pandemic era data to fully answer this question.

The authors' finding that the pandemic predominantly affected cancer yields for certain populations-Asian women-as well as Hispanics and Blacks, is especially troubling. The pandemic has exposed deep fault lines of inequity in our healthcare system. If the observed screening and cancer diagnosis gaps lead to longer-term prognostic consequences, then this may turn out to be yet another way in which the pandemic inequitably affects distinct groups.

The findings of this study therefore serve as a wake-up call for action to ensure that all women of all races and ethnicities have the opportunity to return to timely screening.

Limitations of this article stem from its short-term analysis of outcomes that may ultimately have only finite relevance. While modeling studies have predicted long-term pandemic effects on cancer stage at diagnosis and even on mortality-for example, one study calculated a 0.52% cumulative increase over expected breast cancer deaths by 2030 (10)-it is not possible to truly assess the continued impact of the COVID-era screening moratorium until we can actually observe its later consequences. Eijkelboom and colleagues, for example, found a decrease in screen-detected cancers and specifically a decrease predominantly in lower stage tumors as would be expected. However, as of August 2020 and the restart of screening in the Netherlands, there were no shifts toward higher tumor stage at diagnosis. The organization of the Dutch national screening program likely allows for a more controlled and efficient recapture of women who missed their screens than may be possible in many practices in the United States. In fact, women in the Netherlands who had missed their screening were methodically invited to come in for screening first (6) . It is therefore conceivable that the I n p r e s s consequences and duration of impact of the pandemic on breast cancer outcomes will vary by setting.

In summary, the COVID-19 pandemic has led to a natural experiment, allowing evaluation of the effects of a temporary cessation of screening on breast cancer outcomes. Lowry and colleagues offer a first step to assessing the effects of COVID-19 disruption on cancer detection. Ultimately, the effects of the pandemic on the cancer stage at diagnosis, patient prognosis, and breast cancer mortality are what are most clinically meaningful and for this we will need longer-term national data. It is to be hoped that the authors will continue to report their follow-up observations for this cohort, enabling a more complete understanding of the downstream effects of the pandemic. 

The American Society of Breast Surgeons and The American College of Radiology. Joint Statement on Breast Screening Exams During the Covid-19 Pandemic

Recommendations for prioritization, treatment, and triage of breast cancer patients during the COVID-19 pandemic. the COVID-19 pandemic breast cancer consortium

Prioritizing breast imaging services during the COVID pandemic: A survey of breast imaging facilities within the Breast Cancer Surveillance Consortium

Breast Biopsy Recommendations and Breast Cancers Diagnosed During the COVID-19 Pandemic

Changes in Mammography Use by Women's Characteristics During the First 5 Months of the COVID-19 Pandemic

Impact of the suspension and restart of the Dutch breast cancer screening program on breast cancer incidence and stage during the COVID-19 pandemic

A failure analysis of invasive breast cancer: most deaths from disease occur in women not regularly screened

Outcome analysis for women undergoing annual versus biennial screening mammography: a review of 24,211 examinations

Breast Tumor Prognostic Characteristics and Biennial vs Annual Mammography, Age, and Menopausal Status

Impact of the COVID-19 Pandemic on Breast Cancer Mortality in the US: Estimates From Collaborative Simulation Modeling