In numerous health systems cancer screening programs were among the first activities interrupted by the COVID-19 pandemic after its irruption in early 2020. As reported in a survey by the International Cancer Screening Network, 97% of participating settings reported that COVID-19 had adversely impacted their screening programs, while 90% partially suspended their activity (Puricelli Perin et al., 2021; World Health Organization, 2020). Even in countries with notable success in containing the pandemic, like Taiwan, the population attending screening decreased during the first half of 2020 (Peng et al., 2020).

In Europe, breast cancer screening is mostly provided through organized programs offering routine mammography examination to women aged from 45–50 to 69–74 years. The programs follow the guidelines of the European Commission Initiative for Breast Cancer Screening and Diagnosis (The European Commission’s science and knowledge service, 2020). These guidelines recommend an evidence-based set of performance indicators to evaluate the quality of the screening provision (Muratov et al., 2020). The suspension of these programs led to a reduction in cancer diagnoses. For instance, in the Netherlands and Austria, the number of breast cancer diagnoses decreased substantially and remained lower than expected until screening was rebooted (Dinmohamed et al., 2020; Tsibulak et al., 2020), while in Italy, between January and May 2020, 53% fewer screens were performed, with a median delay of 2.7 months for screening mammograms (Mantellini et al., 2020).

Currently, the evidence of the effect of the COVID-19 pandemic on breast cancer screening performance indicators has been mostly provided by simulation models and longitudinal studies are scarce. In Canada, Yong et al. used a mathematical model to estimate that a 3-month halt would have led to 664,000 fewer screening mammograms than expected, based on nationwide data from the previous year. It would also have decreased breast cancer diagnoses by 7% in 2020 and caused 110 excess deaths by 2029 (Yong et al., 2021). Similar models in Italy reported that 8125 breast cancer diagnoses were expected to be delayed due to a 3-month interruption of screening programs, representing 25% of the 32,500 yearly screening diagnoses nationwide (Vanni et al., 2020).

Spain was one of the first and most affected countries in Europe during the spring of 2020 (Gallo et al., 2021; Karlinsky and Kobak, 2021). On March 14, a general lockdown was enforced, and breast cancer screening was interrupted (Alfonso Viguria and Casamitjana, 2021). Restrictive measures were slowly withdrawn during the following 3 months until June 21, when the lockdown ended (La Vanguardia, 2021). To reintroduce the screening programs as soon as possible while continuing to control the risk of COVID-19 transmission, mammography centers established new safety guidelines (Maio et al., 2021; Pediconi et al., 2020).

Given the scarcity of longitudinal studies, we used a before-and-after design including data from a population-based program from 2012 to 2021. We aimed to assess the impact of the COVID-19 pandemic on the performance indicators of the program of Parc de Salut Mar (PSMAR) of Barcelona, Catalonia, Spain.

Participation in the program was affected differently depending on the type of screening. The aOR of participation between the post- and pre-COVID-19 periods was 0.90 (95% CI = 0.84–0.96) for the group of first-time invitees. The aOR was 1.10 (95% CI = 1.01–1.20) for the previous nonparticipant group between the post- and pre-COVID-19 periods. For the group of women who had participated in the previous round (regular participants), the aOR of participation was 0.63 (95% CI = 0.59–0.67), and for those not participating in the last round (irregular participants), the aOR was 0.95 (95% CI = 0.86–1.05) (Figure 1).

Figure 1

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We also found statistically significant differences in the distribution of baseline characteristics of participants during the post-COVID-19 round compared with the mean distributions of the pre-COVID-19 period (Table 2). The percentage of participants younger than 55 years decreased (−1.64%) but the percentage aged between 55 and 59 years increased (+1.73%). The percentage of participants from high socioeconomic level areas slightly decreased (−0.62%). The biggest changes in the distribution of participants were seen between types of screening, with a substantial decrease among participants in the incident screening group (−2.39%) and an increase in the percentage of prevalent screening, especially first-time invitees (+1.96%). The percentage of participants with a family history of breast cancer increased by 2.53%.

Analysis of participation proportions in different groups according to their characteristics revealed that participation decreased with age, with the largest reduction in participation occurring in women older than 65 years (−3.65%). Although participation decreased among all socioeconomic levels, the decrease was greater in those with middle-low (−6.03%) and low (−5.61%) status. Participation was greatly reduced among regular participants, who had participated in the previous round, with a 4.41% reduction, and slightly increased among previous nonparticipants, who participated for the first time despite having been previously invited (+0.69%) (Table 3).

Analysis of recall revealed modest decreases in the odds of being advised to undergo additional testing during the post-COVID-19 period in both the prevalent and the incident screening groups (aOR = 0.74 [95% CI = 0.56–0.99] and aOR = 0.80 [95% CI = 0.68–0.95]). The aOR of a false positive result for prevalent and incident screening was 0.92 (95% CI = 0.66–1.28) and 0.72 (95% CI 0.59–0.88), respectively. The aOR of cancer detection in the post-COVID vs. the pre-COVID-19 period was 1.01 (95% CI = 0.56–1.71) and 0.87 (95% CI = 0.63–1.17) in the prevalent and incident screening groups, respectively (Figure 2).

Figure 2

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Compliance with recall did not significantly change in the post-COVID-19 round (OR = 1.26, 95% CI = 0.76–2.23), remaining stable with more than 97% of the women advised to undergo further assessment by taking additional diagnostic tests in our facilities (Table 4).

When differentiating between cancer histology, we found no statistically significant reductions in the odds of being diagnosed with a carcinoma in situ (aOR 0.74 [95% CI = 0.32–1.47]) or an invasive tumor (aOR 0.95 [95% CI = 0.70–1.26]), whereas the aOR for all tumors was 0.91 [95% CI = 0.69–1.18] (Figure 3). Finally, we observed no statistically significant differences in the distribution of the tumor size, lymphatic invasion, the presence of metastasis or stage at diagnosis between the pre- and post-COVID-19 periods. A statistically nonsignificant decrease of 4.47% in in situ tumors, and a nonsignificant increase of 4.95% in stages I were noted (Table 5).

Figure 3

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None of the crude results significantly differed from the adjusted results (Supplementary file 1).

In this before-and-after study, we found that the pandemic reduced participation, but also that this impact differed according to each woman’s history of participation. The frequency of recall for additional tests after mammography and the percentage of false-positive results were also significantly lower for incident screening, while for prevalent screening the reduction was only statistically significant for recall. Nevertheless, we found no significant differences in compliance with recall or cancer detection rate.

Women who became eligible for invitation to our population-based screening program for the first time in the post-COVID-19 period were significantly less likely to participate during the pandemic. This effect was also noted, and in a much higher degree, in women who had participated in the previous round. A reduction in participation, although nonstatistically significant, was also seen in women with previous irregular participation. Even though we could not identify the exact reasons behind the lower participation, we hypothesize that possible factors could be general insecurity related to attending hospitals, governmental restrictions of movement, fear of COVID-19 infection, and other uncertainties about the safety of participating in the screening process. This hypothesis is supported by data from a Danish study reporting that two of the reasons for postponing or canceling mammography appointments during the first year of the pandemic were fear and lack of clear guidance on the safety of screening (Kirkegaard et al., 2021).

Women who had been previously invited but had never attended our screening invitation seemed to participate slightly more during the pandemic period. The increase in participation was not expected since this group of women is that with the lowest participation in our setting (Rodriguez et al., 1995). However, this change could be explained by a plausible modification in attitudes to screening with a possible increase in health consciousness promoted by the pandemic, prompting women who had never been interested in screening to participate for the first time. Women who have never previously participated due to private screening may also have switched to the population-based program due to the effect of the pandemic on private clinics, which also had to stop their preventive care programs during lockdown.

Since the invitation process was adapted to the pandemic, the changes in participation could be related to the different strategies used to invite previous participants and nonparticipants. Nevertheless, previous research in our program showed that participation increased with invitation through direct contact with women (Segura et al., 2001), which could be comparable to telephone calls. This effect seemed to be especially relevant in low socioeconomic status areas, where there are more regular participants. Telephone reminders have also been proved to increase participation in different settings, although they usually follow a preset invitation date by postal mail (Duffy et al., 2017). Considering this evidence, we would assume that, without the telephone call, the decrease in participation could have been greater among regular participants. For previous nonparticipants, it is unlikely that an open invitation letter instead of a preset appointment could increase participation. Research in cervical cancer screening has proved that preset appointments increase participation in comparison to open invitations (Lönnberg et al., 2016), and therefore we believe that the increase in participation can be more feasibly explained by the previously discussed changes in private care and health consciousness.

Overall, our findings on participation adjusted by age and socioeconomic status showed that the effect of the pandemic on screening attendance depended on each woman’s previous participation status. Although the aim of our study was not to evaluate the factors associated with participation, we found a lower representation of high-income women in the post-COVID-19 period, but this could probably be explained by the demographic changes in the invited population. Indeed, although participation decreased among all socioeconomic groups, this decline was greater in low-income areas. A systematic review of studies conducted before the pandemic reported lower participation in low-income groups, immigrants, nonhomeowners, and women with a previous false-positive result (Mottram et al., 2021). Furthermore, studies recently published in the United States have reported a decrease in participation, especially in underserved ethnic groups, with lower socioeconomic status, lack of insurance and longer travel time (Amram et al., 2021; Miller et al., 2021). Monitoring this information would allow programs to make efforts to promote participation among women at higher risk of not participating, especially under disruptive situations.

Despite the lower participation, the remaining performance indicators in our program did not seem to be negatively affected by the pandemic. Our results showed a statistically significant reduction in the recall rates of both prevalent and incident screening. These findings could be due to the increased workload caused by COVID-19 patients at our and many other hospitals, which strongly affected the radiology department in 2020 (Posso et al., 2020). We feared that repeat visits to the hospital might be perceived as increasing the risk of COVID-19 exposure, dissuading some women from undergoing any further testing after mammography. However, our data show that compliance with recall remained stable, indicating that women who chose to participate in the first place also engaged with further assessment when advised to do so.

Regarding the frequency of false positives, we found a statistically significant reduction in incident screening and no significant variation in prevalent screening. Considering that false positives and recall are closely related, these results are coherent if no changes in cancer detection rates were to be expected. Since recall and false positives are ideally supposed to be as low as possible, our results suggest that the diagnostic accuracy of the radiologists reading the mammograms was not materially affected by the pandemic. Similar pieces of evidence of the resilience of our public healthcare system have been recently reported in other hospitals in Barcelona (Manzanares et al., 2021), suggesting the strong resilience of health professionals working in critical situations. The COVID-19 pandemic has proved to be a stress test for healthcare systems around the world and the main elements related to highly effective responses have been associated with adaptation of health systems’ capacity, reduction of vulnerability, preservation of healthcare functions and resources, and activation of comprehensive responses (Haldane et al., 2021).

We found no differences in the odds of screen-detected cancer for either prevalent or incident screenings when comparing the pre- and post-COVID-19 periods. In contrast to our statistical approach to estimate the cancer detection as the number of tumors per 1000 participants, when the absolute number of diagnoses during the interruption of the screening programs was compared with previous periods, an evident reduction was observed. A study performed in Málaga (Spain) reported that the breast was one of the cancer sites showing a larger decline in cases in April 2020 compared with April 2019. The authors of that study stated that this decline could be explained by the interruption of the screening program (Ruiz-Medina et al., 2021). Similar results have been found in studies from the Netherlands, Austria, and the United Kingdom (Dinmohamed et al., 2020; Tsibulak et al., 2020; Limb, 2021).

It is still unknown whether the target strategies to reduce the back-log of women who missed screening due to the pandemic, such as contacting them by telephone calls to schedule an appointment, will help to detect cancers missed during screening disruption. The possible influence of the delay on stage at diagnosis needs further evaluation. Although we found no statistically significant differences between pre- and post-COVID-19 periods in our small sample, we did find a small 5% increase in cases diagnosed at stage II. Similarly, an increased risk of late-stage breast cancer was observed in a month-by-month comparison in Israel in the period following the interruption and restoration of the screening activity (Lloyd et al., 2021). Further investigation on stage at diagnosis is essential, especially considering the potential increase in interval cancers due to the delay in the planned mammogram schedule. Moreover, the reduction in participation could increase cancer detection and stage at diagnosis in the next screening round among women who skipped the postpandemic round, leaving a span of 4 years between consecutive screenings.

Our study has some limitations. First, since some women could still have participated after the end of data collection, there could be a small bias overestimating the reduction in participation. Our experience shows that, except for very rare exceptions, women participate in the 3 months following the invitation, a period which was respected for all women in our study. Consequently, we believe the potential effect of this bias to be minimal for the results of our study. Second, the number of cancers detected during the pandemic period was relatively low, which limited the statistical power of our results and did not allow for multilevel models for this outcome. Nevertheless, we believe that, since cancer can only be detected once per woman, the nonindependence of the observations would not have a significant effect on this outcome.

Our study also has some strengths. To our best knowledge, most of the observational evidence assessing the effect of the pandemic compared screening indicators with the previous year (Song et al., 2021; Chen et al., 2021; Toyoda et al., 2021). In contrast, we included a long period of four previous rounds (8 years) of invitations for the same target population. We took this longitudinal approach since it is known that there are fluctuations in participation and cancer detection that may depend on time (Giordano et al., 2015). Therefore, our approach provides information on the pandemic beyond these common fluctuations. We also used a multilevel approach to our analyses in order to account for the nonindependence of the observations, and also provided stratified results according to each woman’s previous history of participation.

In conclusion, our findings suggest that the impact of the pandemic on screening attendance depends on the type of screening, with women who regularly participate being the most affected. Targeting this specific population with a proactive invitation could be a way to ensure the historically higher participation in this group. Despite this, we should not forget other groups that attended screening less frequently. Our program has proved to be resilient, reducing recall and false positives while maintaining invitations and the cancer detection rate stable. These results suggest that the roll-out of the program was successful under the stressful situation provoked by the pandemic. Further prospective research is necessary to assess whether other factors played a role in participation during the pandemic, as well as to better characterize the impact of delays on stage at diagnosis and the incidence of interval cancers.

Source data form all tables and figures can be found in the following Dataset: BOSCH, GUILLERMO, 2022, "Breast cancer screening program invitations (2012-2021)", https://doi.org/10.7910/DVN/VVQNWM, Harvard Dataverse, V1, UNF:6:CaW3sEp4tMsg13z2I1eZbQ == [fileUNF] Data from "Impact on covid19 dataset invited women.sav" was used in tables 1 and 2 and figures 1,2 and 3. Data from "cancer characteristics database.tab" was used in table 3.

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Author details

1. Guillermo Bosch

   1. Department of Epidemiology and Evaluation,IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain
   2. Preventive Medicine and Public Health Training Unit PSMar-ASPB-UPF, Barcelona, Spain

   Contribution

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

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5862-0913

2. Margarita Posso

   1. Department of Epidemiology and Evaluation,IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain
   2. Research Network on Chronicity, Primary Care and Health Promotion (RICAPPS), Barcelona, Spain

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Validation, Writing – original draft, Writing – review and editing

   For correspondence

   mposso@parcdesalutmar.cat

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-5053-257X

3. Javier Louro

   1. Department of Epidemiology and Evaluation,IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain
   2. Research Network on Chronicity, Primary Care and Health Promotion (RICAPPS), Barcelona, Spain

   Contribution

   Data curation, Formal analysis, Investigation, Methodology, Validation, Writing – review and editing

   Competing interests

   No competing interests declared

4. Marta Roman

   1. Department of Epidemiology and Evaluation,IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain
   2. Research Network on Chronicity, Primary Care and Health Promotion (RICAPPS), Barcelona, Spain

   Contribution

   Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Supervision, Writing – review and editing

   Competing interests

   No competing interests declared

5. Miquel Porta

   1. Universitat Autònoma de Barcelona, Barcelona, Spain
   2. Hospital del Mar Institute of Medical Research (IMIM PSMar), Barcelona, Spain
   3. Spanish Consortium for Research on Epidemiology and Public Health (CIBERESP), Madrid, Spain

   Contribution

   Formal analysis, Investigation, Methodology, Supervision, Writing – review and editing

   Competing interests

   No competing interests declared

6. Xavier Castells

   1. Department of Epidemiology and Evaluation,IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain
   2. Research Network on Chronicity, Primary Care and Health Promotion (RICAPPS), Barcelona, Spain
   3. Universitat Autònoma de Barcelona, Barcelona, Spain

   Contribution

   Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Supervision, Writing – review and editing

   Competing interests

   No competing interests declared

7. Francesc Macià

   1. Department of Epidemiology and Evaluation,IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain
   2. Research Network on Chronicity, Primary Care and Health Promotion (RICAPPS), Barcelona, Spain

   Contribution

   Conceptualization, Formal analysis, Investigation, Methodology, Project administration, Supervision, Validation, Writing – review and editing

   Competing interests

   No competing interests declared

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