The impact of the COVID-19 pandemic on Italian population-based cancer screening activities and test coverage: Results from national cross-sectional repeated surveys in 2020
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Curated by eLife
eLife assessment
This paper provides important evidence for the impact of the COVID-19 pandemic on cancer screening for breast, cervix, and colorectal cancer in Italy. The authors compared Invitation and examination coverage, as well as conducted telephone interviews, investigated the population screening test coverage, before and during the pandemic, according to educational attainment, perceived economic difficulties and citizenship. Their findings convincingly show that the lockdown and pandemic restrictions caused delays in screening activities but particularly increased the pre-existing individual and geographical inequalities in access.
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Abstract
In Italy, regions have the mandate to implement population-based screening programs for breast, cervical, and colorectal cancer. From March to May 2020, a severe lockdown was imposed due to the COVID-19 pandemic by the Italian Ministry of Health, with the suspension of screening programs. This paper describes the impact of the pandemic on Italian screening activities and test coverage in 2020 overall and by socioeconomic characteristics.
Methods:
The regional number of subjects invited and of screening tests performed in 2020 were compared with those in 2019. Invitation and examination coverage were also calculated. PASSI surveillance system, through telephone interviews, collects information about screening test uptake by test provider (public screening and private opportunistic). Test coverage and test uptake in the last year were computed by educational attainment, perceived economic difficulties, and citizenship.
Results:
A reduction of subjects invited and tests performed, with differences between periods and geographical macro areas, was observed in 2020 vs. 2019. The reduction in examination coverage was larger than that in invitation coverage for all screening programs. From the second half of 2020, the trend for test coverage showed a decrease in all the macro areas for all the screening programs. Compared with the pre-pandemic period, there was a greater difference according to the level of education in the odds of having had a test last year vs. never having been screened or not being up to date with screening tests.
Conclusions:
The lockdown and the ongoing COVID-19 emergency caused an important delay in screening activities. This increased the preexisting individual and geographical inequalities in access. The opportunistic screening did not mitigate the impact of the pandemic.
Funding:
This study was partially supported by Italian Ministry of Health – Ricerca Corrente Annual Program 2023 and by the Emilian Region DGR 839/22.
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Author Response
Reviewer #1 (Public Review):
This is an interesting and timely paper investigating the impact on participation in cancer screening programs across Italy during the COVID-19 pandemic where there was massive disruptions to health services. What is of particular interest in this analysis was the investigation of social, educational and cultural factors that might have impacted access and participation to screening.
- In the present study, the authors analyzed data collected by PASSI between 2017 and 2021, from interviews of more than 106,000 people, a representative sample of the Italian population aged 25-69 was selected but its not clear what was the representativeness by region, gender and age educational attainment? Also what is the total population (so I don't have to look it up). I am wondering if participation …
Author Response
Reviewer #1 (Public Review):
This is an interesting and timely paper investigating the impact on participation in cancer screening programs across Italy during the COVID-19 pandemic where there was massive disruptions to health services. What is of particular interest in this analysis was the investigation of social, educational and cultural factors that might have impacted access and participation to screening.
- In the present study, the authors analyzed data collected by PASSI between 2017 and 2021, from interviews of more than 106,000 people, a representative sample of the Italian population aged 25-69 was selected but its not clear what was the representativeness by region, gender and age educational attainment? Also what is the total population (so I don't have to look it up). I am wondering if participation differed by characteristics and what approach to achieving the representative sample was made (e.g. replacement of individuals or oversampling certain strata where participation was lower).
PASSI is one of the two routinely collected Italian National Health Interviews. It has been described in several papers and there is a website reporting in detail methods, percentage of refusals, and numbers of interviews. Nevertheless, we agree with the reviewer that a brief summary of the methods is needed, and we added some details on data collection. Furthermore, details on the number of interviews according to the selected period, age, and sex strata cannot be found in the general description of the survey. Therefore, we gave more details also on the sample used for this study in supplementary table 1.
- For figures 5-8 what is the N for the different groups not just the %?
We agree with the reviewer that giving the actual numbers on which the percentages are computed is necessary. Nevertheless, as with any stratified sample, estimates from PASSI are computed using weights, therefore percentages cannot be computed directly from the observed numbers. We decided to add supplementary table 1, which reports the number of valid interviews on which percentages are estimated.
- Table 2 to me is a key piece of information and very interesting can the authors formally test if there are significant differences between the time periods?
Thank the reviewer for this suggestion. Firstly, we added a table in which we analyzed all the data together and we included the calendar period, categorized as before and after the pandemic, among covariates. Secondly, we checked if any of the differences between the prevalence ratios observed in the two periods were significantly different at a 0.05 alpha error threshold and we added a comment in the text: “Nevertheless, the differences could be due to random fluctuations”. We did not add p-values for the interaction of all the variables in each cancer screening because the table is already very complex, and three more columns would make it difficult to read.
Reviewer #3 (Public Review):
This study is primarily a descriptive analysis that provides a clear and accessible account of how screening activity varied across Italy and between groups. While primarily a simple descriptive account such work is important to document what were the impacts of the pandemic on preventative health services and to understand how they differed across groups. The combination of survey responses from regional screening programmes and individuals is a useful use of two data sources. The study is very clearly written and does not over-interpret the presented data.
The methods description states that the analysis presents the "standard months" required for the programmes to recover from the service delays. The subsequent reporting of these delays in the results section did not use the same terminology and I see scope for clarification by using common language regarding this assessment throughout the paper. I see scope for further disaggregation of the regional results within the study but equally I understand why the authors might not wish to report outcomes for specific regions. I see scope for improvement in the figures within the manuscript but this is a relatively presentational matter. I would like to see some further description of the Poisson regression analysis as what is included within the manuscript appears rather brief. There is also one section of the methods that seems as if it would better belong in the introduction, but overall the manuscript was very clearly structured.
We thank the reviewer for his encouraging comments. We checked all the manuscript and we tried to use always the same name for each concept.
We expanded the method section giving more details on models and statistical analysis. We decided not to report data at the regional level but the variability within macro areas.The analysis presented achieves the authors' stated aims in my view. I see a useful contribution in documenting the impact of the COVID-19 pandemic on screening in Italy. This may inform further work on assessing the eventual health impact of delays as well as work considering how best to make screening programmes more resilient to such shocks. Ultimately it will take time to observe just how significant the impacts of service interruptions were on cancer prevention. Readers should remember that many screening services may still provide good protection against cancer as long as the interruptions are limited to simply to delays in coverage rather than the longer-term loss of participation, especially for those with incomplete screening histories or of otherwise elevated risk of disease.
Further work may wish to consider how programmes prioritised capacity or what efforts have been made to restart screening. Similarly, there is scope for more detailed disaggregation assessment of who received screening as programs restarted. Both these issues are beyond the scope of the present study however. The present submission provides a good basis for any further such exploration.
We thank the reviewer for these comments. We tried to capture some of the concepts in our discussion.
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eLife assessment
This paper provides important evidence for the impact of the COVID-19 pandemic on cancer screening for breast, cervix, and colorectal cancer in Italy. The authors compared Invitation and examination coverage, as well as conducted telephone interviews, investigated the population screening test coverage, before and during the pandemic, according to educational attainment, perceived economic difficulties and citizenship. Their findings convincingly show that the lockdown and pandemic restrictions caused delays in screening activities but particularly increased the pre-existing individual and geographical inequalities in access.
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Reviewer #1 (Public Review):
This is an interesting and timely paper investigating the impact on participation in cancer screening programs across Italy during the COVID-19 pandemic where there was massive disruptions to health services. What is of particular interest in this analysis was the investigation of social, educational and cultural factors that might have impacted access and participation to screening.
- In the present study, the authors analyzed data collected by PASSI between 2017 and 2021, from interviews of more than 106,000 people, a representative sample of the Italian population aged 25-69 was selected but its not clear what was the representativeness by region, gender and age educational attainment? Also what is the total population (so I don't have to look it up). I am wondering if participation differed by …
Reviewer #1 (Public Review):
This is an interesting and timely paper investigating the impact on participation in cancer screening programs across Italy during the COVID-19 pandemic where there was massive disruptions to health services. What is of particular interest in this analysis was the investigation of social, educational and cultural factors that might have impacted access and participation to screening.
- In the present study, the authors analyzed data collected by PASSI between 2017 and 2021, from interviews of more than 106,000 people, a representative sample of the Italian population aged 25-69 was selected but its not clear what was the representativeness by region, gender and age educational attainment? Also what is the total population (so I don't have to look it up). I am wondering if participation differed by characteristics and what approach to achieving the representative sample was made (e.g. replacement of individuals or oversampling certain strata where participation was lower).
- For figures 5-8 what is the N for the different groups not just the %?
- Table 2 to me is a key piece of information and very interesting can the authors formally test if there are signficant differences between the time periods?
-
Reviewer #2 (Public Review):
Giorgi Rossi et al measured in their paper the impact of COVID-19 pandemic on the main indicators used to assess the performance of national screening programs for cancers. As expected, they highlighted a significant reduction that changed during the different waves and also across geographical areas. The results of the study might be considered valid and representative as the study is relied on current data flows to assess the performance of screening programs. The paper also reports a complementary analysis on the factor associated to the access to screening that gives some more insights on the reasons behind the access. This second part of the work also relied on data collected at national level that anyway have some intrinsic limitations. Nevertheless, on the whole, the paper gives a useful contribution …
Reviewer #2 (Public Review):
Giorgi Rossi et al measured in their paper the impact of COVID-19 pandemic on the main indicators used to assess the performance of national screening programs for cancers. As expected, they highlighted a significant reduction that changed during the different waves and also across geographical areas. The results of the study might be considered valid and representative as the study is relied on current data flows to assess the performance of screening programs. The paper also reports a complementary analysis on the factor associated to the access to screening that gives some more insights on the reasons behind the access. This second part of the work also relied on data collected at national level that anyway have some intrinsic limitations. Nevertheless, on the whole, the paper gives a useful contribution to the assessment of the disruption due to the pandemic that can be also used in the light of preparedness actions.
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Reviewer #3 (Public Review):
This study is primarily a descriptive analysis that provides a clear and accessible account of how screening activity varied across Italy and between groups. While primarily a simple descriptive account such work is important to document what were the impacts of the pandemic on preventative health services and to understand how they differed across groups. The combination of survey responses from regional screening programmes and individuals is a useful use of two data sources. The study is very clearly written and does not over-interpret the presented data.
The methods description states that the analysis presents the "standard months" required for the programmes to recover from the service delays. The subsequent reporting of these delays in the results section did not use the same terminology and I see …
Reviewer #3 (Public Review):
This study is primarily a descriptive analysis that provides a clear and accessible account of how screening activity varied across Italy and between groups. While primarily a simple descriptive account such work is important to document what were the impacts of the pandemic on preventative health services and to understand how they differed across groups. The combination of survey responses from regional screening programmes and individuals is a useful use of two data sources. The study is very clearly written and does not over-interpret the presented data.
The methods description states that the analysis presents the "standard months" required for the programmes to recover from the service delays. The subsequent reporting of these delays in the results section did not use the same terminology and I see scope for clarification by using common language regarding this assessment throughout the paper. I see scope for further disaggregation of the regional results within the study but equally I understand why the authors might not wish to report outcomes for specific regions. I see scope for improvement in the figures within the manuscript but this is a relatively presentational matter. I would like to see some further description of the Poisson regression analysis as what is included within the manuscript appears rather brief. There is also one section of the methods that seems as if it would better belong in the introduction, but overall the manuscript was very clearly structured.
The analysis presented achieves the authors' stated aims in my view. I see a useful contribution in documenting the impact of the COVID-19 pandemic on screening in Italy. This may inform further work on assessing the eventual health impact of delays as well as work considering how best to make screening programmes more resilient to such shocks. Ultimately it will take time to observe just how significant the impacts of service interruptions were on cancer prevention. Readers should remember that many screening services may still provide good protection against cancer as long as the interruptions are limited to simply to delays in coverage rather than the longer-term loss of participation, especially for those with incomplete screening histories or of otherwise elevated risk of disease.
Further work may wish to consider how programmes prioritised capacity or what efforts have been made to restart screening. Similarly, there is scope for more detailed disaggregation assessment of who received screening as programmes restarted. Both these issues are beyond the scope of the present study however. The present submission provides a good basis for any further such exploration.
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