Cervical cancer screening improvements with self-sampling during the COVID-19 pandemic

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    eLife assessment

    This paper is of interest to researchers and policy makers involved in cervical cancer prevention. The paper provides insight into how the Covid19 pandemic accelerated changes in organized cervical cancer screening. The claim that self-sampling led to a major improvement of test coverage seems somewhat exaggerated and alternative hypotheses to those provided by the authors on the population who chose self-sampling are possible. Nonetheless, this is a valuable piece of work given the scope of the intervention(s) and the precedent it sets i.e. a crisis can in fact accelerate positive changes in screening that have been academic possibilities rather than practical realities.

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Abstract

At the onset of the COVID-19 pandemic cervical screening in the capital region of Sweden was canceled for several months. A series of measures to preserve and improve the cervical screening under the circumstances were instituted, including a switch to screening with HPV self-sampling to enable screening in compliance with social distancing recommendations.

Methods:

We describe the major changes implemented, which were (1) nationwide implementation of HPV screening, (2) switch to primary self-sampling instead of clinician sampling, (3) implementation of HPV screening in all screening ages, and (4) combined HPV vaccination and HPV screening in the cervical screening program.

Results:

A temporary government regulation allowed primary self-sampling with HPV screening in all ages. In the Stockholm region, 330,000 self-sampling kits were sent to the home address of screening-eligible women, instead of an invitation to clinician sampling. An increase in organized population test coverage was seen (from 54% to 60% in just 1 year). In addition, a national campaign for faster elimination of cervical cancer with concomitant screening and vaccination for women in ages 23–28 was launched.

Conclusions:

The COVID-19 pandemic necessitated major changes in the cervical cancer preventive strategies, where it can already be concluded that the strategy with organized primary self-sampling for HPV has resulted in a major improvement of population test coverage.

Funding:

Funded by the Swedish Association of Local Authorities and Regions, the Swedish Cancer Society, the European Union’s Horizon 2020 Research and Innovation Program, the Swedish government, and the Stockholm county.

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  1. Author Response

    eLife assessment

    This paper is of interest to researchers and policy makers involved in cervical cancer prevention. The paper provides insight into how the Covid19 pandemic accelerated changes in organized cervical cancer screening. The claim that self-sampling led to a major improvement of test coverage seems somewhat exaggerated and alternative hypotheses to those provided by the authors on the population who chose self-sampling are possible. Nonetheless, this is a valuable piece of work given the scope of the intervention(s) and the precedent it sets i.e. a crisis can in fact accelerate positive changes in screening that have been academic possibilities rather than practical realities.

    Thank you for this supportive summary. We have included exact data on exactly how much of the population test coverage that was attributable to self-samples. We have furthermore decided to focus on the population test coverage that is caused by organised testing (either taken by a clinician at a time and place that the woman was invited to by the organised program or taken by the woman herself using a sampling kit mailed to her by the organised program). These 2 improved analyses are intended to facilitate interpretation of how much of the improved test coverage that is attributable to the mailing of self-sampling kits.

    Reviewer #1 (Public Review):

    During the Covid19 pandemic, most cervical cancer screening programs were temporarily put on hold. The authors describe how Swedish health authorities dealt with this situation by implementing primary self-sampling and by launching a campaign with concomitant vaccination and screening. Besides, they show that the coverage of the screening program was one year after the start of the pandemic at pre-pandemic levels.

    Strengths of the paper are the clear presentation of the steps taken by the Swedish health authorities and the high quality of the presented screening coverage data which could be obtained directly from the screening registry. However, the paper would benefit from more in-depth analyses because the presented data raise questions. The number of invitations was >30 percent lower in the first year of the pandemic (Figure 1), but the screening coverage was only 4-5 percent lower. In the second year of the pandemic (year 2021), coverage was back at pre-pandemic levels, but the role of primary self-sampling in restoring screening coverage is a bit unclear. It is obvious that primary self-sampling made it possible to invite women again for screening during the pandemic, but there is no data on acceptance of primary self-sampling. Besides, the increase in coverage in year 2021 was only 4% and it is not clear whether such a modest increase could also have been achieved without primary self-sampling. In addition to self-sampling, the authors describe the launch of a concomitant vaccination and screening campaign. This is an interesting initiative but the authors do not show data on the coverage of this campaign in the target age range.

    We are now explaining that population test coverage is calculated over a whole screening interval. For example, if the screening interval is 3 years and improved attendance would only fully impact the population test coverage after 3 years. Furthermore, we are now presenting the exact data on how much of the test coverage is indeed attributable to the mailing of self-sampling kits.

    Reviewer #2 (Public Review):

    The manuscript by Elfstrom et al describes the impact of implementing self-sampling as the primary screening test in Sweden to address decreases in coverage following the COVID pandemic. The authors have a very rich dataset including all records of invitations to screen and screening results in the Stockholm area. A limitation is that there is no individual record linkage to allow investigation of the profile of the individuals who chose to screen using the self-sample.

    The conclusions are generally well supported by the authors with the following exceptions:

    1. There was not enough evidence presented in the manuscript to conclude that "The most likely explanation for the large increase in population coverage seen is that the sending of self-sampling kits resulted in improved attendance in particular among previously non-attending women."
    1. The authors state there is no evidence that delays in screening have impacted cervical cancer rates however they present no data to this effect in the manuscript.

    Although all screening and invitation data is indeed collected to the national screening registry, linking this data is not allowed without a permission from the Swedish National Ethical Review Board. We did apply for such a permission, which was granted on 2023-02-01, and a full set of registry linkage analyses to investigate the point raised by the reviewer is now included.

    The mention in discussion on stable cervical cancer rates was referring to public data from the national Cancer Registry. The source is now referenced.

    Reviewer #3 (Public Review):

    The authors report on the nature of interventions that were applied to aid and improve engagement in cervical screening, brought about by the SARS CoV Pandemic in Sweden.

    I appreciate that the impact of these interventions, given that they are recent, will take some time to quantify but the description (and reach) of the policy changes that occurred in a short amount of time is of significant interest to the screening community. The piece on HPV Even Faster is particularly novel; I am not aware of another example of where this has been enacted within a routine programme.

    Thank you for this supportive statement.

    The authors make reference to (15) where the reader can find greater details relating to the population who received the offer of self sampling (and the nature of the device). However I was a little confused (in this stand alone piece) as to who the self sampling group constituted exactly. Did this group not include pregnant women, women invited for first screen or women on non routine recall?

    This is correct, self-sampling kits were mailed to all women due for screening in the ages 26-70. Women due for screening aged 23-25 were invited for mid-wife-based sampling. Pregnant women were advised to come in for mid-wife-based screening, to save time. Women under follow-up from previous screens are not due for screening. This is now elaborated more clearly in the paper.

    The authors state that "the most likely explanation for the large increase in population coverage seen is that the sending of self-sampling kits resulted in improved attendance in particular among previously non-attending women" - why is this written as speculation at this stage (?) is it not possible to attribute directly the contribution made by self sampling, or is this in hand?

    See response to reviewer 2 above: Although all the data is indeed collected, we are not allowed to perform registry linkages without ethical permission. This has now been obtained and the requested analyses made.

    While self sampling is certainly an option that can support uptake and enfranchisement in cervical screening - its overall performance is fundamentally contingent on the number of women who then comply with follow up should the HPV test be positive; it is not simply about who returns the sample. It would have been of interest to see the proportion of women who did comply with follow up.

    The paper is not about follow-up strategies. Follow-up strategies are different in different settings and reporting is not standardized. They have also changed during the time of the study (e.g. cytology follow-up abandoned). A more detailed analysis of this would require a whole new paper.

  2. eLife assessment

    This paper is of interest to researchers and policy makers involved in cervical cancer prevention. The paper provides insight into how the Covid19 pandemic accelerated changes in organized cervical cancer screening. The claim that self-sampling led to a major improvement of test coverage seems somewhat exaggerated and alternative hypotheses to those provided by the authors on the population who chose self-sampling are possible. Nonetheless, this is a valuable piece of work given the scope of the intervention(s) and the precedent it sets i.e. a crisis can in fact accelerate positive changes in screening that have been academic possibilities rather than practical realities.

  3. Reviewer #1 (Public Review):

    During the Covid19 pandemic, most cervical cancer screening programs were temporarily put on hold. The authors describe how Swedish health authorities dealt with this situation by implementing primary self-sampling and by launching a campaign with concomitant vaccination and screening. Besides, they show that the coverage of the screening program was one year after the start of the pandemic at pre-pandemic levels.

    Strengths of the paper are the clear presentation of the steps taken by the Swedish health authorities and the high quality of the presented screening coverage data which could be obtained directly from the screening registry. However, the paper would benefit from more in-depth analyses because the presented data raise questions. The number of invitations was >30 percent lower in the first year of the pandemic (Figure 1), but the screening coverage was only 4-5 percent lower. In the second year of the pandemic (year 2021), coverage was back at pre-pandemic levels, but the role of primary self-sampling in restoring screening coverage is a bit unclear. It is obvious that primary self-sampling made it possible to invite women again for screening during the pandemic, but there is no data on acceptance of primary self-sampling. Besides, the increase in coverage in year 2021 was only 4% and it is not clear whether such a modest increase could also have been achieved without primary self-sampling. In addition to self-sampling, the authors describe the launch of a concomitant vaccination and screening campaign. This is an interesting initiative but the authors do not show data on the coverage of this campaign in the target age range.

  4. Reviewer #2 (Public Review):

    The manuscript by Elfstrom et al describes the impact of implementing self-sampling as the primary screening test in Sweden to address decreases in coverage following the COVID pandemic. The authors have a very rich dataset including all records of invitations to screen and screening results in the Stockholm area. A limitation is that there is no individual record linkage to allow investigation of the profile of the individuals who chose to screen using the self-sample.

    The conclusions are generally well supported by the authors with the following exceptions:

    1. There was not enough evidence presented in the manuscript to conclude that "The most likely explanation for the large increase in population coverage seen is that the sending of self-sampling kits resulted in improved attendance in particular among previously non-attending women."

    2. The authors state there is no evidence that delays in screening have impacted cervical cancer rates however they present no data to this effect in the manuscript.

  5. Reviewer #3 (Public Review):

    The authors report on the nature of interventions that were applied to aid and improve engagement in cervical screening, brought about by the SARS CoV Pandemic in Sweden.

    I appreciate that the impact of these interventions, given that they are recent, will take some time to quantify but the description (and reach) of the policy changes that occurred in a short amount of time is of significant interest to the screening community. The piece on HPV Even Faster is particularly novel; I am not aware of another example of where this has been enacted within a routine programme.

    The authors make reference to (15) where the reader can find greater details relating to the population who received the offer of self sampling (and the nature of the device). However I was a little confused (in this stand alone piece) as to who the self sampling group constituted exactly. Did this group not include pregnant women, women invited for first screen or women on non routine recall?

    The authors state that "the most likely explanation for the large increase in population coverage seen is that the sending of self-sampling kits resulted in improved attendance in particular among previously non-attending women" - why is this written as speculation at this stage (?) is it not possible to attribute directly the contribution made by self sampling, or is this in hand?

    While self sampling is certainly an option that can support uptake and enfranchisement in cervical screening - its overall performance is fundamentally contingent on the number of women who then comply with follow up should the HPV test be positive; it is not simply about who returns the sample. It would have been of interest to see the proportion of women who did comply with follow up.