The COVID-19 pandemic has had a significant impact on cancer screening programs around the world. Numerous countries worldwide have reported varying degrees of reductions in participation (1–5). For example, in comparison to 2019, Slovenia saw a 92% decline in cytology volume between March and May 2020 (6), while Belgium experienced a 43% reduction in volume between January and April 2020 (7). Meanwhile, the United States reported a 92% decrease in participation compared to 2019 during March and April 2020 (8). In Peru, a 76% reduction in cytology volume was observed for 2020 compared to the expected volume based on modeled data (9)

In Spain, a nationwide lockdown was imposed on March 14th 2020. All cancer preventive services, including cervical cancer screening, were suspended, and only follow-up appointments for previous abnormal results were maintained (10). The lockdown was gradually lifted between May 11^th and June 2020 (11), and primary screening in Catalonia was partially resumed in July 2020. In the two years since the pandemic began, six COVID-19 waves have occurred. Containment measures for these waves have varied across and within Spanish regions, including social distancing or mobility restriction within residential areas, although exceptions were made for medical visits.

The medium- and long-term impact of these disruptions on cervical cancer is still uncertain although Mexico has observed an increasing trend in the proportion of advanced stage and metastatic cancer cases (12). In Catalonia, the COVID-19 pandemic and related control measures have resulted in cancer underdiagnosis (13–15). In the two years since the lockdown, 11% fewer cervical cancers have been diagnosed, and as of February 2022, cervical cancer detection in Catalonia had not yet returned to pre-pandemic levels (15). The potential impact on the cancer stage is unknown. However, no differences have been observed in the prevalence of cancer diagnoses in pathology records from 2019 and 2020 in two hospitals in Girona (16).

When the pandemic began, Catalonia was offering opportunistic cytology-based cervical cancer screening to women aged 25 to 65 through the public primary care system. The first pandemic wave hit when the transition from cytology-based to HPV-based screening on clinician-collected samples had just begun through a pre-scale-up pilot in an area of Barcelona city on October 2019 (17). Therefore, a significant consequence of the pandemic in Catalonia was the interruption and delay in the transition to primary HPV testing that was underway. To date, HPV testing has not yet been extended to the entire territory due to the pandemic, which prompted the development of a newly organized cervical cancer screening program based on self-sampling. This new strategy aimed to counteract the reduced number of scheduled visits to facilitate social distancing and the lower willingness of potential participants to visit a health center after the lockdown period. Accordingly, a pilot program for HPV testing of self-collected samples was launched in July 2021 in Metropolitana Sud, a metropolitan area in the south of Barcelona city (18).

A better understanding of the post-lockdown screening landscape can help inform decisions on the best catch-up strategies for under screened women. However, only some studies have explored the impact of the pandemic beyond the lockdown period. Germany reported a lower average number of women screened per clinic in 2021 than in 2020 (19). In the United States, despite a rebound in the third quarter of 2020, a slow decline in screening rates has been observed up to the last quarter of 2021 (20).

The pandemic has likely led to longer screening intervals between cervical cancer screenings, as observed for breast and colorectal cancer screening in Belgium (21). However, the same study also found that there were either no differences or shorter screening intervals in cervical cancer screening during the pandemic compared to before, probably due to the opportunistic screening and follow-up tests done during the lockdown. Women with longer screening intervals have a higher risk of disease and therefore higher prevalences of abnormal cytology or biopsy results are expected. In Brazil, the prevalence of abnormal cytology findings remained unchanged overtime; however, in 2020 and 2021, the CIN3 prevalence doubled compared to the 1.9% observed in 2019 (22). Other studies have only explored changes in the number of cases, and as observed with cancer diagnoses, underdiagnosis of high-grade cytologies and CIN2+ cases have been described in Slovenia and Canada, respectively (6, 23).

We evaluated the impact of the COVID-19 pandemic on opportunistic screening participation, abnormal cytology prevalence, and screening intervals within the Catalan public health system throughout the first two years after the pandemic started (period 2020–2021) using primary care electronic health records data.

We performed a time-series analysis of 2020 and 2021 on the participation, abnormal cytology prevalence and screening interval in the opportunistic cervical cancer screening program of Catalonia.

In Catalonia, after the lockdown period due to the COVID-19 pandemic, lower participation in cervical cancer opportunistic screening was observed in 2020 and 2021, although it highly improved in 2021. Participation was lower at increasing ages. Since the pandemic, a higher abnormal cytology prevalence and a larger screening interval have also been observed.

During the lockdown period in Catalonia, there was up to a 96% reduction in participation to cervical cancer screening in April 2020. Similarly, others have reported the highest impact in April 2020 with similar estimates (7, 8, 28). However, pooled data from other studies worldwide show the most significant reduced cervical cancer screening participation in March 2020 (5), whereas in Slovenia and Japan, it took place in May 2020 (6, 29). The start and end of lockdown periods had likely played a role when the highest reduction was observed.

In 2020, 39% fewer women (47% if the first two months without contentious measures implemented are excluded from the analysis) participated in cervical cancer screening in Catalonia. Different countries have described lower participation or screening test volumes (2–5). However, the impact estimate highly depends on the reported period, which hampers a straight comparison with others. The impact of COVID-19 in Catalonia over the 12 months period of 2020 was higher than the 23% lower cytology volume reported in Slovenia over a 7-month period in the same year (6) and the 36% lower screening estimated for the United States over a 9-month period, also in 2020 (8). However, it was less severe than the 76% reduction in cytology volume observed in Peru over the same 12-month period (9). Overall, in 2021, 2% fewer women participated in cervical cancer screening because of the reduced participation in January (24% reduction) as the third epidemic wave took place and mobility restrictions were again implemented. However, these mobility restrictions did not prohibit attendance to cancer screening visits. Therefore, this lower participation might be related to changes in women’s attitude towards self-care behavior, such as the self-reported lower willingness to attend cervical cancer screening and the perception that screening tests were not urgent in the United Kingdom (30, 31) or the observed longer time to help-seeking for cancer symptoms in Spain (32) after the first COVID-19 pandemic wave. Except for January, observed participation in 2021 was not different than expected, as opposed to the lower estimates observed in Germany and the United States (19, 20).

At an increasing age, Catalonia observed a more considerable impact in screening participation and a slower recovery in regular participation. Lower participation at increasing age was also observed in Slovenia (6), whereas a larger impact was observed in England at young ages (33). The higher impact in women aged 55–65 years than those younger might be related to a higher self-perceived risk of getting severe COVID-19 if infected by the SARS-CoV2 virus at older ages and willingness to avoid contact with the health system unless symptomatic.

The COVID-19 pandemic in Catalonia has not only affected the still opportunistic cervical cancer screening activities. Lower participation in organized cancer screening programs in the region has also been observed for breast (34) and colorectal (35) cancer screening programs. A lower number of diagnoses have also been observed in other chronic diseases managed at primary care services, such as asthma or ischemic heart disease (36).

A higher prevalence of abnormal cytology was observed after the lockdown period (up to 1.5 times higher than expected). The validation of the predictive models with 2014 - 2018 data showed an increasing trend in abnormal cytologies prevalence before the pandemic, yet it was used to adjust the expected prevalences for 2020 and 2021. It follows that the previously observed trend does not explain the observed higher prevalence of abnormal cytology during the pandemic. In Brazil, the prevalence of abnormal cytology findings remained unchanged in the years 2020 and 2021 but, in São Paulo city, the CIN3 prevalence increased (4.5% in 2020 and 3.8% in 2021) in comparison with the 1.9% CIN3 prevalence in 2019 (22). The authors argue that the increase in CIN3 might be related to the follow-up of 2019 abnormal cytology results. Ours is the first study to measure an increase in cytology abnormal prevalence since the pandemic started although we cannot assess whether this increase in cytology abnormality has resulted in an increase in CIN2+ prevalence.

Another potential explanation for the higher prevalence could be related to a larger screening interval. The longer the period after a normal screening result, the lower assurance that the patient remains disease-free and, therefore, a greater prevalence of abnormal cytology results. In our study, we have observed an increasing median time since the last normal cytology from June 2020 onwards among all women and a longer interval in those with an abnormal cytology result compared to those with a normal one. To our knowledge, only one study has explored the cervical cancer screening interval with contrasting findings to our study. In Belgium, no differences in the screening interval were observed between the pre-pandemic and pandemic periods (21). The authors attribute this to the opportunistic screening activity and the follow-up tests done during the lockdown period. In contrast, we excluded follow-up tests from the analyses to accurately estimate the median time since the last screening test, which was 48 months by December 2021.

According to modeling studies, COVID-19-related screening delays have a lower impact on the lifetime cervical cancer risk than the screening test used and the screening frequency (37). Another study estimated that the risk of cervical cancer is higher in women missing the screening round, i.e., those being screened, although with a longer screening interval. Therefore, catch-up campaigns using HPV testing have been suggested to address this issue (38). However, due to a potentially limited capacity in screening organizations, others have estimated that the best balance between screening capacity and health impact is to ensure that women are screened, even if it is done at a longer interval (39). This is consistent with the increased risk observed in women that missed their round (i.e., a delay in screening participation equal to the screening interval) than those that were screened at a longer screening interval (40). However, in Catalonia, cervical cancer screening is still opportunistic and, as a result, women at higher risk (longer time since their last screening) are not identified and offered to screen. Therefore, we are currently piloting the implementation of self-sampling methods in an organized cervical cancer screening program aiming to increase screening capacity and to offer screening to those under screened. However, its scale-up has been slowed down.

In this study, we highlight using predictive models to estimate the expected participation in 2020 after validating our model with expected versus observed data in 2019 instead of assuming constant participation as in previous years. It is also noteworthy to mention that using the SISAP database facilitates the reporting of objective data (others have reported data facilitated by questionnaires to health managers) known to be highly representative of the whole Catalan population. Despite the strengths, our study has some limitations that need to be mentioned. Although changes in participation, abnormal cytology prevalence and screening interval coincide with the COVID-19 pandemic, we cannot rule out other reasons for such changes due to the use of ecological data to study the potential association between our findings and the COVID pandemic. One of these reasons could be that more women use private health services during the pandemic, so participation has been maintained in the overall population but decreased in the public health sector. However, our analysis database only contains data from the latter. On the other hand, the lack of access to structured histology data has prevented us from exploring whether the increase in abnormal cytology prevalence has been translated in an increase in CIN2+ prevalence.

The COVID-19 pandemic has significantly impacted cervical cancer screening in Catalonia, resulting in decreased screening participation, longer screening intervals and a potentially related increase in abnormal cytology prevalence. Therefore, close monitoring of the potential increases in cervical cancer diagnosis or the changes in cancer stage at diagnosis is warranted. Furthermore, to prevent a further increase in advanced cervical cancer diagnosis, it is crucial to expedite the implementation of the organized HPV-based screening program in Catalonia.

The data analyzed in this study is subject to the following licenses/restrictions: It contains health records. Requests to access these datasets should be directed to crobles@iconcologia.net.

The studies involving humans were approved by Ethics Committee from the Hospital Universitari de Bellvitge. The studies were conducted in accordance with the local legislation and institutional requirements. Written informed consent for participation was not required from the participants or the participants’ legal guardians/next of kin in accordance with the national legislation and institutional requirements.

CR: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Writing – original draft, Writing – review & editing. LM: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing. RI: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Writing – review & editing. ER: Conceptualization, Data curation, Investigation, Methodology, Writing – review & editing. RF: Data curation, Resources, Writing – review & editing. PP-T: Methodology, Writing – review & editing. MB: Methodology, Writing – review & editing. CM-B: Resources, Writing – review & editing. SS: Methodology, Writing – review & editing. JE: Data curation, Resources, Writing – review & editing. LB: Conceptualization, Data curation, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Writing – review & editing.