Prior to the COVID-19 pandemic outbreak in spring 2020, the Swedish cervical cancer prevention efforts consisted of invitations for screening at maternity clinics at an interval of 3–7 years. The National Board of Health and Welfare decided in 2015 that screening of 30- to 70-year-old women should primarily be performed with an HPV test and screening of 23- to 29-year-old women with cytology (National Board of Health and Welfare, 2015). However, 5 years later when surveyed during the autumn of the pandemic, 5/21 regions in Sweden had still not implemented the national program. Self-sampling targeting long-term non-attenders as a method to increase population coverage was recommended but was rarely used (Swedish National Cervical Screening Registry, 2021). There was school-based vaccination of both girls and boys (with high population coverage) (National Board of Health and Welfare, 2022) but no consideration of strategies for an even faster strategy to eliminate cervical cancer by concomitant screening and vaccination of young women (Dillner et al., 2021). Although HPV testing has been shown to have higher sensitivity in all age groups and higher specificity for women aged 30 or older compared to cytology-based screening, it was previously not recommended below 30 years of age largely because of the high prevalence of HPV infections, most of which will be cleared without causing cellular lesions or cancer, leading to overdiagnosis and overtreatment (Arbyn et al., 2012; Leinonen et al., 2009; Ronco et al., 2014). However, an increasing proportion of young women that are entering the screening program have been vaccinated, resulting in lower HPV prevalences and lower predictive values of screening (Lei et al., 2020b). Cellular abnormalities among young, vaccinated women are still seen, but typically contain only non-progressive HPV types (Kann et al., 2020).

In April of 2020 all non-emergency healthcare was stopped in the capital region of Sweden because of a severe COVID-19 outbreak. Consequently, 192,000 cervical cancer screening invitations with appointments were canceled. In June the same year, the screening program was allowed to restart but the midwife clinics could not be used for screening as usual, to avoid crowding. The Swedish National Board of Health and Welfare enacted a temporary regulation that (1) allowed for primary self-sampling instead of clinician-based sampling and (2) allowed for primary HPV-based screening in all ages between 23 and 70 years of age. It is well known that when self-samples are analyzed using an HPV assay based on polymerase chain reaction, the sensitivity is not inferior to samples taken by medically trained staff (Arbyn et al., 2018) and that self-sampling can be used to increase population coverage of screening, with improved attendance among under-screened and hard-to-reach women (Elfström et al., 2019; Winer et al., 2019).

The number of cervical screening invitations sent per month in the Stockholm region during 2019 and 2020 is shown in Figure 1. The formal decision to cancel all screening was effective April–June 2020, during which time there was a severe COVID-19 outbreak in the Stockholm region (Pimenoff et al., 2021). When screening was re-initiated in the second half of 2020, only a limited number of invitations were allowed per screening station in order to avoid crowding (Figure 1). During the second half of 2020, only women invited for their first cervical screen and women due for follow-up after abnormal screening results were invited to clinician sampling. Clinician-based sampling was also recommended for women who were pregnant when they received their invitation to self-sampling. There were preparations for a switch to primary self-sampling as the prime screening modality, which was launched in March 2021. Except for women at first cervical screen, pregnant women and follow-up after abnormal screens, self-sampling kits were mailed to all eligible women in the population (direct send instead of invitation to maternity care clinic – no requirement of having to order the kit). A detailed description of the self-sampling kits and their use can be found in Elfström et al., 2019.

Figure 1

Download asset Open asset

The organized screening program is based on first generating a list of eligible women who (1) are resident in the catchment area (in this case the greater Stockholm region, with about 2 million resident inhabitants), (2) did not take a cervical test during the recommended age-specific screening interval (3 years 23–49 years of age, 7 years 50–70 years of age). This is assessed by importing of files with tests performed from all laboratories (both public and private) in the region and comparing the sampling dates and the personal identification numbers with the population registry of resident women (3) checking that they did not opt out of the screening program. This is not common, but out of the 732,276 resident women in the eligible target ages, 2655 women (0.4%) had opted out of the program. In the switch that was implemented in March 2021, the previous policy of sending an invitation letter with an appointment time for cervical screening at a local Maternity Care clinic was for most women (see above) replaced by sending of a self-sampling kit (including instructions and a pre-paid return envelope). During 2021, approximately 320,000 self-sampling kits were mailed. There was an increase in the population coverage of the organized cervical screening program, from 54% to 60% (Table 1). The improvement was seen in most age groups and the population test coverage levels approached the test coverage levels in the year before the COVID-19 outbreak when the program was canceled (Table 1). There has been a steady increase in population test coverage over the past decade (Figure 2). The trend was broken during the pandemic, but the trend seems to be restored in 2021 (Figure 2).

Figure 2

Download asset Open asset

Because population test coverage is calculated over the length of a full screening interval, most of the population test coverage was still attributable to tests taken already before the pandemic. As shown in Table 2, about two thirds of the coverage was still attributable to clinician-based sampling also in the age groups 26–70 where there had been no possibility for organized screening using clinician taken samples (except for pregnant women) since the start of the pandemic.

As Sweden uses an annual call & recall system, a certain proportion of the population test coverage is attributable to participation by previous non-attenders (Table 3). The proportion of the test coverage that was attributable to long-term non-attenders taking self-samples was 3.9%, a large part of the overall increase in population test coverage seen (Table 3). Note that self-samples were not used at all before 2019 and were used only in a small scale project targeting non-attenders in 2019–2020 (Table 3).

The increased attendance using self-sampling among prior non-attenders is particularly evident when population coverage is expressed as a proportion of the sampling mode (Table 4). Whereas the proportion of the test coverage attributable to clinician sampling of prior non-attenders has always been less than 10% of the samples, >20% of the population test coverage attributable to self-sampling was attributable to prior non-attenders (Table 4).

As self-sampling cannot be used for cytology, only for HPV testing, the need to use self-sampling promoted a change to more widespread use of HPV testing. Although HPV testing had been mandated from age 30 and upwards already in 2015, in 2020 there were still 5 counties that did not use it. This changed and since autumn 2021 all counties in Sweden now use primary HPV screening. In the age groups below 30, HPV screening had not previously been recommended because of concerns about over-screening in an age where HPV infections were common. However, HPV prevalences are dropping because of vaccination and the emergency interim guidelines had now allowed HPV screening in all ages.

After the pandemic, permanent regulations were issued that came into effect on 2022-07-01. These allow choice between primary self-sampling and sampling by a clinician and have also changed the age for HPV screening to be mandated between 23 and 70 years of age. In other words, the changes that were required because of the pandemic have resulted in that huge and permanent improvements could be implemented.

A large COVID-19 outbreak in the Stockholm region necessitated concentration of healthcare to emergency care and cancer screening was canceled. We describe that the major measures taken to mitigate the screening deficit (organized primary self-sampling and an even faster campaign with concomitant screening and vaccination) resulted in several important and lasting improvements of the cervical cancer prevention program in Sweden.

The roll-out of primary self-sampling was done in the context of routine screening which means that decisions were made consecutively and the program was adapted as needed to meet the changing dynamics of the pandemic. Therefore, this analysis of the response was completed post hoc. Given that Sweden has a comprehensive registry of all invitations (including mailing of self-sampling materials) and all cervical tests performed in the country, it was possible to perform a detailed description and evaluation of the switch retrospectively. The national even faster campaign with concomitant screening and vaccination was launched as a formal Phase IV trial with the protocol registered at clinicaltrials.gov where everyone interested can read the details.

In the US, there was a 94% reduction of cervical cancer screenings during the initial phase of the pandemic compared to the same period the previous years, and although the screening has partially recovered since then, the cervical cancer screening rates are still 10% below pre-pandemic levels (Mast et al., 2022). Likewise, in England a 43–91% drop per month of received screening samples was observed during the period April to June 2020 and by April 2021 there was still 6.4% fewer samples than expected (Castanon et al., 2022). Thus, although there was a prompt re-initiation of screening through re-opening of screening services and catch-up screening during the period following the initial phase of the pandemic, the impact of the disruption was significant. This contrasts with our findings where the disruption was used as an opportunity to advance the program, with lasting improvements already materializing as a greatly improved screening coverage, lower costs of sample taking and increased use of HPV vaccines.

Self-sampling in cervical screening is well known to improve participation among women who seldom or never attended screening (Sultana et al., 2016). The increase in population coverage seen is at least in part due to that the sending of self-sampling kits resulted in improved attendance in particular among previously non-attending women.

As the cancellation of non-emergency healthcare also involved canceling of follow-up and treatment of newly detected screen-positive women, it has been speculated that a rise in cervical cancer would result (Castanon et al., 2022; Daniels et al., 2021). We could, however, not see any such effect in incidence data from the Swedish Cancer Registry (https://www.socialstyrelsen.se/), probably because non-emergency healthcare was allowed again in June 2020 after a less than 3 months disruption.

In summary, the major COVID-19 outbreak necessitated several emergency changes to the cervical screening program. These have resulted in several major and lasting improvements of the cervical cancer prevention strategy that are likely to promote an accelerated elimination of HPV and cervical cancer.

The data in this report derive from publicly available data on new Swedish regulations and strategies used during the pandemic (major official websites https://www.socialstyrelsen.se/ and https://www.regeringen.se/). Results on population coverage and number of screening invitations/self-sampling kits sent are derived from the website of the Swedish National Cervical Screening Registry of Sweden (https://www.nkcx.se/).

1. 1. Apter D
   2. Wheeler CM
   3. Paavonen J
   4. Castellsagué X
   5. Garland SM
   6. Skinner SR
   7. Naud P
   8. Salmerón J
   9. Chow S-N
   10. Kitchener HC
   11. Teixeira JC
   12. Jaisamrarn U
   13. Limson G
   14. Szarewski A
   15. Romanowski B
   16. Aoki FY
   17. Schwarz TF
   18. Poppe WAJ
   19. Bosch FX
   20. Mindel A
   21. de Sutter P
   22. Hardt K
   23. Zahaf T
   24. Descamps D
   25. Struyf F
   26. Lehtinen M
   27. Dubin G
   28. HPV PATRICIA Study Group

   (2015) Efficacy of human papillomavirus 16 and 18 (HPV-16/18) AS04-adjuvanted vaccine against cervical infection and precancer in young women: final event-driven analysis of the randomized, double-blind PATRICIA trial

   Clinical and Vaccine Immunology 22:361–373.

   https://doi.org/10.1128/CVI.00591-14

   • PubMed
   • Google Scholar
2. 1. Arbyn M
   2. Ronco G
   3. Anttila A
   4. Meijer C
   5. Poljak M
   6. Ogilvie G
   7. Koliopoulos G
   8. Naucler P
   9. Sankaranarayanan R
   10. Peto J

   (2012) Evidence regarding human papillomavirus testing in secondary prevention of cervical cancer

   Vaccine 30 Suppl 5:F88–F99.

   https://doi.org/10.1016/j.vaccine.2012.06.095

   • PubMed
   • Google Scholar
3. 1. Arbyn M
   2. Smith SB
   3. Temin S
   4. Sultana F
   5. Castle P
   6. Collaboration on Self-Sampling and HPV Testing

   (2018) Detecting cervical precancer and reaching underscreened women by using HPV testing on self samples: updated meta-analyses

   BMJ 363:k4823.

   https://doi.org/10.1136/bmj.k4823

   • PubMed
   • Google Scholar
4. 1. Bosch FX
   2. Robles C
   3. Díaz M
   4. Arbyn M
   5. Baussano I
   6. Clavel C
   7. Ronco G
   8. Dillner J
   9. Lehtinen M
   10. Petry K-U
   11. Poljak M
   12. Kjaer SK
   13. Meijer CJLM
   14. Garland SM
   15. Salmerón J
   16. Castellsagué X
   17. Bruni L
   18. de Sanjosé S
   19. Cuzick J

   (2016) HPV-FASTER: broadening the scope for prevention of HPV-related cancer

   Nature Reviews. Clinical Oncology 13:119–132.

   https://doi.org/10.1038/nrclinonc.2015.146

   • PubMed
   • Google Scholar
5. 1. Castanon A
   2. Rebolj M
   3. Pesola F
   4. Pearmain P
   5. Stubbs R

   (2022) COVID-19 disruption to cervical cancer screening in England

   Journal of Medical Screening 29:203–208.

   https://doi.org/10.1177/09691413221090892

   • PubMed
   • Google Scholar
6. 1. Daniels V
   2. Saxena K
   3. Roberts C
   4. Kothari S
   5. Corman S
   6. Yao L
   7. Niccolai L

   (2021) Impact of reduced human papillomavirus vaccination coverage rates due to COVID-19 in the United States: A model based analysis

   Vaccine 39:2731–2735.

   https://doi.org/10.1016/j.vaccine.2021.04.003

   • PubMed
   • Google Scholar
7. 1. Dillner J
   2. Elfström KM
   3. Baussano I

   (2021) Prospects for accelerated elimination of cervical cancer

   Preventive Medicine 153:106827.

   https://doi.org/10.1016/j.ypmed.2021.106827

   • PubMed
   • Google Scholar
8. 1. Elfström KM
   2. Sparén P
   3. Olausson P
   4. Almstedt P
   5. Strander B
   6. Dillner J

   (2016) Registry-based assessment of the status of cervical screening in Sweden

   Journal of Medical Screening 23:217–226.

   https://doi.org/10.1177/0969141316632023

   • PubMed
   • Google Scholar
9. 1. Elfström KM
   2. Sundström K
   3. Andersson S
   4. Bzhalava Z
   5. Carlsten Thor A
   6. Gzoul Z
   7. Öhman D
   8. Lamin H
   9. Eklund C
   10. Dillner J
   11. Törnberg S

   (2019) Increasing participation in cervical screening by targeting long-term nonattenders: Randomized health services study

   International Journal of Cancer 145:3033–3039.

   https://doi.org/10.1002/ijc.32374

   • PubMed
   • Google Scholar
10. 1. Kann H
    2. Hortlund M
    3. Eklund C
    4. Dillner J
    5. Faust H

    (2020) Human papillomavirus types in cervical dysplasia among young HPV-vaccinated women: Population-based nested case-control study

    International Journal of Cancer 146:2539–2546.

    https://doi.org/10.1002/ijc.32848

    • PubMed
    • Google Scholar
11. 1. Lei J
    2. Ploner A
    3. Elfström KM
    4. Wang J
    5. Roth A
    6. Fang F
    7. Sundström K
    8. Dillner J
    9. Sparén P

    (2020a) HPV vaccination and the risk of invasive cervical cancer

    The New England Journal of Medicine 383:1340–1348.

    https://doi.org/10.1056/NEJMoa1917338

    • PubMed
    • Google Scholar
12. 1. Lei J
    2. Ploner A
    3. Lehtinen M
    4. Sparén P
    5. Dillner J
    6. Elfström KM

    (2020b) Impact of HPV vaccination on cervical screening performance: a population-based cohort study

    British Journal of Cancer 123:155–160.

    https://doi.org/10.1038/s41416-020-0850-6

    • PubMed
    • Google Scholar
13. 1. Leinonen M
    2. Nieminen P
    3. Kotaniemi-Talonen L
    4. Malila N
    5. Tarkkanen J
    6. Laurila P
    7. Anttila A

    (2009) Age-specific evaluation of primary human papillomavirus screening vs conventional cytology in a randomized setting

    Journal of the National Cancer Institute 101:1612–1623.

    https://doi.org/10.1093/jnci/djp367

    • PubMed
    • Google Scholar
14. Website

    1. Mast C
    2. Deckert J
    3. Munoz del A

    (2022) Troubling cancer screening rates still seen nearly two years into the pandemic: Epic Health Research Network

    Accessed December 12, 2023.

    https://epicresearch.org/articles/troubling-cancer-screening-rates-still-seen-nearly-two-years-into-the-pandemic
15. Book

    1. National Board of Health and Welfare

    (2015)

    Screening for Cervical Cancer - Recommendation and Assessment Documentation

    National Board of Health and Welfare.

    • Google Scholar
16. Book

    1. National Board of Health and Welfare

    (2022)

    Screening for Cervical Cancer

    National Board of Health and Welfare, Stockholm. Sweden.

    • Google Scholar
17. 1. Pimenoff VN
    2. Björnstedt M
    3. Dillner J

    (2021) Severe features during outbreak but low mortality observed immediately before and after a March-May 2020 COVID-19 outbreak in Stockholm, Sweden

    International Journal of Infectious Diseases 110:433–435.

    https://doi.org/10.1016/j.ijid.2021.08.005

    • PubMed
    • Google Scholar
18. 1. Ronco G
    2. Dillner J
    3. Elfström KM
    4. Tunesi S
    5. Snijders PJF
    6. Arbyn M
    7. Kitchener H
    8. Segnan N
    9. Gilham C
    10. Giorgi-Rossi P
    11. Berkhof J
    12. Peto J
    13. Meijer C
    14. International HPV screening working group

    (2014) Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials

    Lancet 383:524–532.

    https://doi.org/10.1016/S0140-6736(13)62218-7

    • PubMed
    • Google Scholar
19. 1. Sultana F
    2. English DR
    3. Simpson JA
    4. Drennan KT
    5. Mullins R
    6. Brotherton JML
    7. Wrede CD
    8. Heley S
    9. Saville M
    10. Gertig DM

    (2016) Home-based HPV self-sampling improves participation by never-screened and under-screened women: Results from a large randomized trial (iPap) in Australia

    International Journal of Cancer 139:281–290.

    https://doi.org/10.1002/ijc.30031

    • PubMed
    • Google Scholar
20. Report

    1. Swedish National Cervical Screening Registry

    (2021) Annual report of the Swedish National Cervical Screening Registry

    Swedish National Cervical Screening Registry.

    https://nkcx.se/templates/_rsrapport_2021.pdf

    • Google Scholar
21. 1. Winer RL
    2. Lin J
    3. Tiro JA
    4. Miglioretti DL
    5. Beatty T
    6. Gao H
    7. Kimbel K
    8. Thayer C
    9. Buist DSM

    (2019) Effect of mailed human papillomavirus test kits vs usual care reminders on cervical cancer screening uptake, precancer detection, and treatment: a randomized clinical trial

    JAMA Network Open 2:e1914729.

    https://doi.org/10.1001/jamanetworkopen.2019.14729

    • PubMed
    • Google Scholar

Author details

1. Miriam Elfström

   1. Center for Cervical Cancer Elimination, F46, Pathology and Cancer Diagnostics, Medical Diagnostics Karolinska, Karolinska University Hospital and Division of Cervical Cancer Elimination, CLINTEC, Karolinska Institutet, Stockholm, Sweden
   2. Regional Cancer Center of Stockholm-Gotland, Cancer Screening Unit, Sweden, Stockholm, Sweden

   Contribution

   Conceptualization, Data curation, Formal analysis, Validation, Investigation, Project administration, Writing – review and editing

   Competing interests

   No competing interests declared

2. Penelope Grace Gray

   Center for Cervical Cancer Elimination, F46, Pathology and Cancer Diagnostics, Medical Diagnostics Karolinska, Karolinska University Hospital and Division of Cervical Cancer Elimination, CLINTEC, Karolinska Institutet, Stockholm, Sweden

   Contribution

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

   Competing interests

   No competing interests declared

3. Joakim Dillner

   Center for Cervical Cancer Elimination, F46, Pathology and Cancer Diagnostics, Medical Diagnostics Karolinska, Karolinska University Hospital and Division of Cervical Cancer Elimination, CLINTEC, Karolinska Institutet, Stockholm, Sweden

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Visualization, Methodology, Writing - original draft, Project administration, Writing – review and editing

   For correspondence

   Joakim.Dillner@ki.se

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8588-6506

• 250

  views

• 63

  downloads

• 2

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.