Breast cancer is the most common cancer worldwide, with 2.3 million cases diagnosed and 685,000 deaths in 2020 (WHO, 2021). Mammography-based screening programs allow for early detection of breast cancers for earlier intervention and disease stage that improves patient outcomes (IARC, 2022). Early detection and diagnosis from screening may reduce mortality by up to 65% among breast cancer patients (Berry et al., 2005). Populations with a good uptake rate in screening programs can achieve a 90% 5-year survival rate in patients who received an early diagnosis attributed to screening (WHO, 2021).

COVID-19 affected global health systems and has strained population breast mammography screening programs. Previous work on modeled evaluations and a focus on tumor staging and mortality as outcomes suggested that scenarios are likely to differ by region and organization of delivery of breast cancer screening (Figueroa et al., 2021). In different countries, screening models vary from population-based to opportunistic screening (offered to patients in healthcare settings – more common in private healthcare) (IARC, 2016).

Here we aimed to quantify systematically breast screening participation rates before and after the first COVID-19 wave amidst the suspensions in nations with/without opportunistic screening programs. This was performed by investigating two primary study outcomes: changes in screening volume and participation uptake rates.

Figure 1 summarizes the search strategy. The initial search retrieved 1207 articles and 935 independent records. After screening (see ‘Methods’), 26 cross-sectional studies from 13 countries were eligible for inclusion (Table 1). We counted Scotland and England as two separate national entities due to the devolved healthcare systems. However, it should be noted that breast screening policies and practice between NHS Scotland and NHS England are similar. In total, 7 reports came from Europe (Campbell et al., 2021; Jidkova et al., 2022; Knoll et al., 2022; Eijkelboom et al., 2021; Losurdo et al., 2022; Toss et al., 2021; NHS England, 2021), 2 from Oceania (BreastScreen Australia, 2020; BreastScreen Aoteroa, 2022), 1 from Asia (Shen et al., 2022), 2 from South America (Bessa, 2021; Ribeiro et al., 2022), and 14 from North America (Chiarelli et al., 2021; Walker et al., 2021; Doubova et al., 2021; Chen et al., 2021; Amornsiripanitch et al., 2021; Becker et al., 2021; DeGroff et al., 2021; Dennis et al., 2021; Fedewa et al., 2021; Lehman et al., 2022; London et al., 2022; Miller et al., 2021; Sprague et al., 2021; Nyante et al., 2021). The most frequently reported country was the USA (n = 11). Studies examined either regional (n = 13) or national populations (n = 13).

Figure 1

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During COVID-19, many countries implemented various mitigation methods to reduce transmission and of course mortality. To summarize these different infection control measures, Table 1 shows that all 13 countries/nations had international movement controls in place, 23 study-specific regions had internal movement controls, 21 study-specific regions had stay-at home requirements in place, 1 study-specific region (Northern Italy, Emilia Romagna) had public transport closures, 23 study-specific regions had bans on gatherings >10 people, 24 study-specific regions had public events bans in place, 24 study-specific regions had workplace closures in place, and 23 study-specific regions had in-person school closures in place (Mathieu, 2022; CIHI, 2022; Commonwealth of Massachusetts, 2021; Commonwealth of Virginia, 2023; Cooper et al., 2023; SPICe, 2023; State of Michigan, 2020; State of North Carolina, 2020).

Analysis of data from all studies was limited from January 1, 2020, to December 31, 2020.

We previously reported on modeled evaluations that estimated short- and long-term outcomes for various scenarios and changes in breast screening volume, uptake rates, and breast cancer diagnosis rates (Figueroa et al., 2021; WHO, 2021). In this rapid review, we show that during COVID-19 there was a generally reported reduction in breast cancer screening volume and participation uptake rate that varied by healthcare setting (e.g., national population-based screening vs. opportunistic or private healthcare). Our data suggests that volume and participation uptake are important metrics that requires monitoring by health systems and could inform prevention and early diagnosis efforts, especially if certain groups are not participating.

Non-pharmaceutical interventions were essential and effective in containing the spread of COVID-19 in the era without vaccines; these extend to domestic/international movement controls, social distancing, and ban on events and gatherings and workplace/school closure (Li et al., 2021; Talic et al., 2021). While these measures were important to reduce the mortality directly related to COVID-19, they also had indirect effects on other health services including breast cancer screening. In this rapid review, we provide evidence that screening volume and participation uptake rates were reduced but this reduction varied by region and healthcare system.

In a systematic review and meta-analysis, data from 72 studies were used to investigate the effectiveness of public health measures in reducing COVID-19 incidence and transmission (Talic et al., 2021). The meta-analysis pooled an estimate from eight studies and indicated that handwashing (Relative Risk (RR): 0.47; 95% CI: 0.19–1.12), mask-wearing (RR: 0.47; 95% CI: 0.29–0.75), and physical distancing (RR: 0.75; 95% CI: 0.59–0.95) were associated with the reduction in COVID-19 incidence. The remaining public health measures including quarantine and isolation, universal lockdowns, and closures of borders, schools, and workplaces which could not be included in the meta-analysis were evaluated in a narrative way. The findings validated the effectiveness of both individual and packages of public health measures on the transmission of SARS-CoV-2 and incidence of COVID-19. However, the majority of included studies had moderate risk of bias based on quality assessment. For breast cancer screening, the importance of mitigation measures that emphasized physical distancing to have been the most important in reducing screening, both for general population participation but also at healthcare facilities aiming to reduce transmission (Figueroa et al., 2021).

Reductions in screening capacity due to physical distancing are likely another source for screening volume reductions. Screening capacity reductions were caused by social distancing, staggered appointments, staff exposure to COVID-19, and cleaning measures. This likely resulted in reductions in time allocated for screening to occur (Walker et al., 2021; Sprague et al., 2021). Sprague et al., 2021 considered screening capacity when assessing screening volume. Even though screening capacity recovered to pre-pandemic levels in July 2020, screening volume experienced a 10.8% decrease relative to the control period. Reductions in screening capacity were potentially not the sole factor to screening volume reductions. However, most publications included in our rapid review did not collect data regarding screening capacity, so we cannot determine the proportion of change in screening volume that was attributed to either reduction in screening capacity or change in patient willingness to attend screening. Future analyses are needed where both measures are obtained, which would inform what measures are needed (e.g., information campaigns to alleviate patient fears or increase clinical staffing for catch-up of missed appointments).

Our data supports differences by healthcare system that were particularly evident in data from the USA where there is a mix of private and national healthcare (Medicare) for persons 65+ [https://www.medicare.gov/]. DeGroff et al., 2021, who studied populations reliant solely on national health insurance, showed larger screening volume reductions (–39.00%). This was relative to studies focusing solely on populations with private insurances or studies including patients from both groups (–36.50 to +30%). Amornsiripanitch et al., 2021, which included national and private insurance patients, corroborate this. Medicaid and Medicare patients had –17.06% screening volume reduction compared to –10.50% experienced by the entire population. Miller et al., 2021 suggest that opportunity cost of attending breast screening in lower income groups (e.g., employment) may have led to decreased breast screening in such populations. Some literature showed increases in screening volumes (Nyante et al., 2021; Becker et al., 2021) and uptake rates (Campbell et al., 2021). Increased volume (+9%) from Nyante et al., 2021 could be inconclusive as the observed screening volume was compared against a modeled 2019 population that was used to simulate a 2020 population in the absence of COVID-19. Although this study was robust, limited data collection till September 2020 did not show full extent of change regarding screening volumes after lifting of COVID-19 suspension guidelines in June 2020. From trends explored in study, breast screening rates were possibly recovering in the study population (USA) in late 2020, but more data is required. The Affordable Care Act may have alleviated breast screening cost through health insurance coverage reforms (Zhao et al., 2020). However, this does not address other underlying socioeconomic inequalities (e.g., high cost of treatment, time off from work due to sickness). Patients from deprived backgrounds may be fearful of dealing with the consequences of abnormal screening results (e.g., treatment). This may strain patient finances worsened by COVID-19, potentially explaining lower screening volumes and uptake. Future data on patient characteristics including insurance status, socioeconomic, and race/ethnicity could inform targeted campaigns to reduce inequities if disparities exist.

Becker et al., 2021 showed a screening volume increase after the lifting of COVID-19 suspension guidelines. This study focused on patients who utilize solely private insurance. Patients already paying for services may be more inclined to maximize utilization of coverage. However, this study states that the odds that a woman received breast cancer screening remained 20% lower in 2020 (OR = 0.80 [0.80, 0.81]) relative to 2019. This study scored poorly in the JBI appraisal tool due to poor outcome measurement; it was unclear how the odds ratio was derived, therefore, increasing the risk of bias of this study. Unusual outcome measures were used, that being the claims invoice for the service. This appeared unreliable; it was unclear whether paying for the service equates to a fulfilled appointment. Invoices could be delayed, making it unclear when the screening took place. This study’s evidence quality needs to be increased for results to be conclusive.

Campbell et al., 2021 state a 10.96% increase in uptake rate in Scotland. This study population (within the study period) solely included patients who had their appointments cancelled in March 2020 due to the first lockdown and high-risk patients. This particular patient group may have an increased urgency to catch up on screening. This could have contributed to the increased uptake rate of screening in Scotland in the study period. The increase in uptake rates could also be attributed to the increased accessibility for patients due to the ‘work-from-home’ model and increased health consciousness due to COVID-19. Neither raw data nor sample size was defined in the study and will require future analysis.

Due to the inherent weaknesses of a rapid review, certain limitations are present within the study as explored below. However, this study can be expanded upon by various means (also explored below) to further elucidate the global impact of COVID-19 on breast cancer detection and subsequent care. Other limitations include COVID-19 context as an evolving field with fast publication turnovers; more papers could have been published since the review started. This issue could be partially addressed by completing a repeat search with employment of forward and backward citation tracking, while including more gray literature sources apart from governmental databases (e.g., private screening databases). Other limitations included studies had insufficient data for combined analysis regarding COVID-19 waves past December 2020. Additionally, the data obtained was cross-sectional instead of cohort-based; we were unable to analyze trends and recovery in breast cancer screening rates and incidence rates over time. Exclusion of non-English-language literature was a weakness. Many countries with extensive population-based breast screening programs that were affected by COVID-19 in Europe and Asia were unaccounted for; the inclusion of additional data would be useful to clarify the impact of the pandemic on breast cancer screening program uptake. Furthermore, it should also be noted that COVID-19 infection rates were not reported by the included studies and data from governmental/health board websites may not report study-specific region infection rates.

In summary, screening volume and uptake rates were generally reduced but many studies showed gains over time even if overall a decline in screening volume was observed. These declines were likely due to the first COVID-19 wave where many healthcare facilities paused non-essential services. Volume and uptake reductions of smaller magnitudes were observed, and our data suggest some difference depending on region and healthcare coverage. Access to screening services may increase marginalization of some vulnerable groups in the USA due to the pandemic, and recovery efforts to reduce disparities in access to screening and early diagnosis should be monitored to determine whether prevention services need strengthening. Participation uptake and volume are not conclusive endpoints themselves, and future work from registries and other data sources are needed to determine whether there has been any impact on incidence, stage, and mortality outcomes.

We performed a rapid review (Tricco et al., 2015), where systematic review processes were modified to facilitate project completion within a shortened timeframe. Searches were limited to two databases and English-language governmental gray literature.

Source data included as Supplementary file 1.

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Author details

1. Reagan Lee

   Usher Institute, University of Edinburgh, Edinburgh, United Kingdom

   Contribution

   Conceptualization, Data curation, Investigation, Methodology, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3658-4103

2. Wei Xu

   1. Usher Institute, University of Edinburgh, Edinburgh, United Kingdom
   2. Centre for Global Health, University of Edinburgh, Edinburgh, United Kingdom

   Contribution

   Data curation, Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0009-0008-3338-4545

3. Marshall Dozier

   Information Services, University of Edinburgh, Edinburgh, United Kingdom

   Contribution

   Data curation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-5151-1252

4. Ruth McQuillan

   Usher Institute, University of Edinburgh, Edinburgh, United Kingdom

   Contribution

   Conceptualization, Supervision, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0998-9540

5. Evropi Theodoratou

   Centre for Global Health, University of Edinburgh, Edinburgh, United Kingdom

   Contribution

   Conceptualization, Supervision, Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

6. Jonine Figueroa

   1. Centre for Global Health, University of Edinburgh, Edinburgh, United Kingdom
   2. Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, United States

   Contribution

   Data curation, Formal analysis, Supervision, Methodology, Writing – original draft, Writing – review and editing

   For correspondence

   jonine.figueroa@ed.ac.uk

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-5100-623X

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