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. 2023 Jan 23;18(1):e0280790. doi: 10.1371/journal.pone.0280790

Participation and adherence to mammography screening in the Capital Region of Denmark: The importance of age over time

Lindsay Pett 1,*,#, Becky Hollenberg 1,#, Jessica Mahoney 1,#, Jake Paz 1,#, Nathan Siu 1,#, Amanda Sun 1,#, Rachel Zhang 1,#, My von Euler-Chelpin 1,#
Editor: Sandar Tin Tin2
PMCID: PMC9870097  PMID: 36689434

Abstract

Mammography screening’s effectiveness depends on high participation levels. Understanding adherence patterns over time is important for more accurately predicting future effectiveness. This study analyzed longitudinal adherence to the biennial invitations in the Capital Region of Denmark from 2008–2017. We analyzed participation rates for five-year age groups along with their percent changes in each invitation round using linear regressions. Participation in the mammography screening program increased from 73.1% to 83.1% from 2008–2017. The participation rate among all age groups increased from the first to the fifth round, with the oldest age group having the largest increase (average percent change = 3.66; p-value = 0.03).

Introduction

Breast cancer, worldwide, is the most common cancer in women and was responsible for more than 600,000 deaths in 2018 [1]. Additionally, breast cancer now causes the highest annual number of cancer deaths in women [1]. Studies have established that mammography screening is an effective tool for reducing breast cancer mortality [25]. However, its effectiveness depends upon high levels of participation in the screening program. The European Guidelines for Quality Assurance in Breast Cancer Screening and Diagnosis recommend that at least 70–75% of a population participate in regular mammography screening [6].

Background

To achieve this goal of high participation, substantial research has been conducted to assess participation in Denmark and numerous other countries. There are personal, socio-economic, as well as cultural differences in adherence to organized mammography screening [2, 714]. Poorer physical and mental health, diminished primary care physician interaction levels, lower social support, lower educational attainment, and older age have been associated with lower levels of adherence [2, 7, 8, 1014]. Several of these possible determinants are also independently related to age. In an earlier study from Denmark, the participation rate was significantly lower in the age group 65–69 than in the age group 50–54 (p<0.0001) [15]. Interventions targeting these groups may promote equal participation in future breast cancer screening programs. Although research has identified many factors that affect participation rates, many of these studies look only at singular screenings or screenings over a few years [714]. Relatively few studies have examined longitudinal adherence by age group across multiple invitation rounds in a national screening program. One longitudinal study from Lithuania examines screening participation rates from 2006–2014, noting that participation increased more than three-fold over this time period [16]. Another such study from Spain found that adherence rates decreased from 2011 to 2017 [17].

We wanted to assess the possible change in participation and adherence by age group over time. To this end, we used data from the Capital Region Mammography Screening Register to analyze time trends and longitudinal adherence to the biennial invitations in the capital region of Denmark from 2008–2017.

Material and methods

Healthcare, and thereby also screening, is free of charge in Denmark. In the Capital Region, breast cancer screening is offered every second year to all women aged 50–69 years. The invitation is personal and women are invited with a fixed, changeable, appointment to visit one of the five mammography screening clinics in the region. Women who do not show up are sent a reminder. Participation, assessment of abnormal findings, and eventual treatment are all free of charge for the women. Women not wanting to participate can opt out of the invitation scheme. Each two-year invitation period is called an invitation round. Women diagnosed with cancer will be eligible for rescreening within the program after approximately 18 months.

For the present study, we retrieved data on all mammography screening examinations from 1 January 2008 to 31 December 2017 from the Capital Region Mammography Screening Register. Data was split by 5-year age groups and stratified by each invitation round. The study is entirely a register study, and no contact was made to the women included in the screening program. Consequently, no approval from the Ethical Committee or informed participant consent was needed according to Danish Law. The project was approved by The Faculty of Health and Medical Sciences under the General Data Protection Regulation, Regulation 2016/679, Ref. no.: 514-0238/18-3000. All data were pseudo-anonymized before use by the authors, and no images were accessed.

Data from this study are stored in Statistics Denmark, which only can be accessed given the relevant data permits in accordance with GDPR and Danish Law. The data is based on personal identification numbers and open access would seriously compromise the privacy of the women included in the study.

Participation was calculated as the number of women who participated in each invitation round divided by the number of women invited for each invitation round and stratified by 5-year age groups. The percent change in participation rates for the five participation rounds were calculated for each age group. The 95% confidence intervals for the participation rates were calculated using Vasser Stats’s confidence interval of a proportion calculator [18]. Joinpoint Regression Program version 4.8.0.1 (2020) [19] was used to run linear regressions of the participation rates within each age group and analyze differences between the slopes. An alpha of p = 0.05 was used for all analyses.

Results

Overall participation in the mammography screening program increased from 73.1% to 83.1% from the first invitation round to the final invitation round (Table 1). In invitation round one, 190,583 women were invited to participate in the mammography screening program. 73.1% of these women participated in screening [95% CI: 73.0, 73.4]. Among the age groups, participation rates ranged from 68.7% in the oldest age group [95% CI: 68.3, 69.2] to 75.2 among the 55–59 age group [95% CI: 74.9, 75.6]. In invitation round two, 185,966 women were invited to participate in the mammography screening program. 72.2% of these women participated in screening [95% CI: 72.1, 72.5]. Among the age groups, participation rates ranged from 71.1% in both the youngest and oldest age groups [Age 50–54 95% CI: 70.8, 71.6; Age 65–69 95% CI: 70.7, 71.5] to 74.3 among the 60–64 age group [95% CI: 74.0, 74.7]. The total percent change in participation rate from round one to round two was -1.23%, ranging from -3.86% in the 55–59 age group to 3.49% in the oldest age group. In invitation round three, 181,475 women were invited to participate in the mammography screening program. 79.9% of these women participated in screening [95% CI: 79.7, 80.0]. Among the age groups, participation rates ranged from 76.4% in the youngest age group [95% CI: 76.1, 76.8] to 82.2 among the 60–64 age group [95% CI: 81.9, 82.6]. The total percent change in participation rate from round two to round three was 10.7%, ranging from 7.5% in the youngest age group to 13.08% in the oldest age group. In invitation round four, 204,315 women were invited to participate in the mammography screening program. 77.7% of these women participated in screening [95% CI: 77.5, 77.9]. Among the age groups, participation rates ranged from 76.6% in the youngest age group [95% CI: 76.3, 77.0] to 79.3 among the 60–64 age group [95% CI: 78.9, 79.6]. The total percent change in participation rate from round three to round four was -2.75%, ranging from -3.95% in the 55–59 age group to 3.53% in the 60–64 age group. In invitation round five, 186,671 women were invited to participate in the mammography screening program. 83.1% of these women participated in screening [95% CI: 82.9, 83.2]. Among the age groups, participation rates ranged from 80.3% in the youngest age group [95% CI: 80.0, 80.6] to 84.7 among the 60–64 age group [95% CI: 84.3, 85.0]. The total percent change in participation rate from round two to round three was 6.95%, ranging from 4.83% in the youngest age group to 8.54% in the oldest age group.

Table 1. Mammography screening invitations and participation in the Capital Region of Denmark from 2008–2017 by age group.

Invitation Round 1 Invitation Round 2 Invitation Round 3 Invitation Round 4 Invitation Round 5
2008–2009 2010–2011 2012–2013 2014–2015 2016–2017
Invited Population Participated (% of invited) [95% CI] Invited Population Participated (% of invited) [95% CI] % Change Invited Population Participated (% of invited) [95% CI] % Change Invited Population Participated (% of invited) [95% CI] % Change Invited Population Participated (% of invited) [95% CI] % Change
AGE 50–54 51833 38182 (73.7) [73.3, 74.0] 49571 35269 (71.1) [70.8, 71.6] -3.53 52634 40237 (76.4) [76.1, 76.8] 7.45 58656 44936 (76.6) [76.3, 77.0] 0.26 59012 47391 (80.3) [80.0, 80.6] 4.83
55–59 46649 35097 (75.2) [74.9, 75.6] 46156 33392 (72.3) [71.9, 72.8] -3.86 43774 35491 (81.1) [80.7, 81.4] 12.17 49007 38187 (77.9) [77.6, 78.3] -3.95 45582 38460 (84.4) [84.0, 84.7] 8.34
60–64 51045 37921 (74.3) [73.9, 74.7] 47447 35276 (74.3) [74.0, 74.7] 0 41200 33885 (82.2) [81.9, 82.6] 10.63 44482 35259 (79.3) [78.9, 79.6] 3.53 40920 34643 (84.7) [84.3, 85.0] 6.81
65–69 41056 28209 (68.7) [68.3, 69.2] 42792 30423 (71.1) [70.7, 71.5] 3.49 43867 35300 (80.5) [80.1, 80.8] 13.08 52170 40310 (77.3) [76.9, 77.6] -3.86 41157 34546 (83.9) [83.6, 84.3] 8.54
Total 190583 139409 (73.1) [73.0, 73.4] 185966 134360 (72.2) [72.1, 72.5] -1.23 181475 144913 (79.9) [79.7, 80.0] 10.66 204315 158692 (77.7) [77.5, 77.9] -2.75 186671 155040 (83.1) [82.9, 83.2] 6.95

Of the 91,988 women invited to all 5 rounds (i.e. women who were alive, living in the Capital region, accepting invitation and in the correct age group), 64.8% attended all five rounds. 32.8% of women attended some of the rounds, and 2.4% attended none of the rounds (Table 2).

Table 2. Mammography screening attendance in the Capital Region of Denmark from 2008–2017.

# Invited to All # Attended All # Attended Some # Attended No
Rounds Rounds (%) Rounds (%) Rounds (%)
91,988 59,625 (64.8%) 30,177 (32.8%) 2,186 (2.4%)

The youngest age group had an average percent change (APC) of 1.87 with a p-value of 0.06, indicating that the APC was not significantly different from zero at the alpha = 0.05 level (Fig 1). The 55–59 age group had an APC of 2.40 with a p-value of 0.11, indicating that the APC was not significantly different from zero at the alpha = 0.05 level. The 60–64 age group had an APC of 2.58 with a p-value of 0.052, indicating that the APC was borderline significantly different from zero at the alpha = 0.05 level. The oldest age group was the only group that had a statistically significant average percent change in participation rate from the first invitation round to the final invitation round. The APC of 3.66 with a p-value of 0.03 indicated that the APC was significantly different from zero at the alpha = 0.05 level. The total regression had an APC of 2.55 with a p-value of 0.0496, indicating that the APC was significantly different from zero at the alpha = 0.05 level.

Fig 1. Linear model of mammography screening participation rates among the four age groups and the total group in the Capital Region of Denmark from 2008–2017 (color needed).

Fig 1

Discussion

We found an increasing participation rate in all age groups over time. The most significant change occurred within the older age groups, who participated to a larger extent than they did before. There can be several explanations for this. Women who chose to opt out of the program were not invited into subsequent rounds, causing the invited population to be selected towards participation. Women in the youngest age group had over time an increased participation, which possibly influenced their adherence as they aged and moved into older age groups. Only the 65-69-year-olds had a participation rate lower than 70% in invitation round 1. However, of all women eligible to all 5 invitation rounds, only 65% participated in all rounds, which is significantly lower than the participation rate in any of the individual rounds. This finding could be problematic, as Andersen’s 2015 study found that continued regular adherence among individuals is needed for optimal protection [20].

A study of Spain’s mammography screening program found that the adherence rate has decreased from 2011 to 2017 among women aged 40–69 [17]. The adherence rate in 2017 was below the recommended 70%. These results contrast with our study that found increasing participation rates in the Capital Region of Denmark well in accordance with the recommended 70%. A cross-sectional study of the Canadian mammography screening program found that participation was highest among the 60–69 age group, followed by the 50–59 age group [14]. Overall participation rate in this study was slightly below the recommended 70%. This is in relative accordance with our results as they found that the younger women participated at a slightly lower rate than older women, but our study had a higher overall participation rate. In Lithuania, the participation rate in their national mammography screening program increased more than three-fold from 2006 to 2014 [16]. Notably, Lithuania’s participation rate at the onset of the program was 20%, significantly lower than in Denmark which began with a rate over the 70% minimum. Another large study examines the participation rates for 17 European Union (EU) countries from 2004–2014 [21]. Most of the countries’ participation rates have slightly decreased since their programs’ inceptions, with the exception of six countries, including Denmark. The other countries with increased participation rates were Belgium, France, Czech Republic, Estonia, and Slovakia. Among these exceptions, Denmark is the only country that has consistently had a participation rate over 70% and has increased significantly since its inception. Examining an age breakdown of these other countries to determine if the age-based participation rates matched our results for the Capital Region of Denmark’s program would provide further insight.

Most population-based mammography screening programs, including the Danish program, treat screening on a “one-size-fits-all” basis, where the only determinant is age. It is quite possible that age may not be the best determinant of participation. Personalized mammography screening, utilizing risk-based screening recommendations, could provide a better alternative to one-size-fits-all mammography screening programs.

A limitation of our study is that participation may be overestimated due to people opting out, creating a selection toward those who want to participate. Another limitation is the short follow-up of only 5 invitation rounds which gives room for natural variation. A strength of our study was that the capital Region Mammography Screening Register with invitation data is known to be nearly 100% complete with a very high degree of accuracy.

Conclusions

The participation rate among all age groups has generally increased from the first round of the Capital Region of Denmark’s mammography screening program to the fifth invitation round. The oldest age group experienced the largest increase in their average participation rate. Complete adherence was lower than the recommended 70%, but while high participation is a requirement for optimal benefit from screening, with age no longer being a stratifying factor, more personalized mammography screening may provide a better alternative to standardized one-size-fits-all programs.

Acknowledgments

We wish to acknowledge the role of DIS Study Abroad, Copenhagen for research assistance.

Data Availability

The data underlying this article cannot be shared for the privacy of the individuals who participated in the mammography screening programs. The data will be shared on reasonable request to the corresponding author. The data are stored in the national bureau of statistics in Denmark, called Statistics Denmark (DST). The data is pseudo-identified, i.e. the Danish personal identification number is switched with another number. However, there is a key between the two which according to Danish law constitutes a risk for potential identification. The data can, with the relevant permissions, be accessed by contacting the Department of Public Health, University of Copenhagen, Denmark with reference to the research project “Benefits and harms of screening for breast cancer with mammography” and through that department potentially gain access to the data at DST. Department of Public Health Faculty of Health and Medical Sciences University of Copenhagen Phone: +45 35 32 76 23 Department contact: George Napolitano, gena@sund.ku.dk https://publichealth.ku.dk/.

Funding Statement

The authors received no specific funding for this work.

References

  • 1.Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018). Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68(6):394–424. 10.3322/caac.21492 . [DOI] [PubMed] [Google Scholar]
  • 2.Barco I, Chabrera C, García Font M, Gimenez N, Fraile M, Lain JM, et al. Comparison of Screened and Nonscreened Breast Cancer Patients in Relation to Age: A 2-Institution Study. Clin Breast Cancer. 2015. Dec;15(6):482–9. doi: 10.1016/j.clbc.2015.04.007 [DOI] [PubMed] [Google Scholar]
  • 3.Bleyer A, Baines C, Miller AB. Impact of screening mammography on breast cancer mortality. Int J Cancer. 2016. Apr 15;138(8):2003–12. doi: 10.1002/ijc.29925 [DOI] [PubMed] [Google Scholar]
  • 4.Hanley JA, Hannigan A, O’Brien KM. Mortality reductions due to mammography screening: Contemporary population-based data. PloS One. 2017;12(12):e0188947. doi: 10.1371/journal.pone.0188947 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Van Ourti T, O’Donnell O, Koç H, Fracheboud J, de Koning HJ. Effect of screening mammography on breast cancer mortality: Quasi‐experimental evidence from rollout of the Dutch population‐based program with 17‐year follow‐up of a cohort. Int J Cancer. 2020. Apr 15;146(8):2201–8. doi: 10.1002/ijc.32584 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.European guidelines for breast cancer screening and diagnosis: the European breast guidelines. [Internet]. Publications Office of the European Union. Publications Office of the European Union; 2017 [cited 2020 Jun 11]. http://op.europa.eu/en/publication-detail/-/publication/b7b66c78-e139-11e6-ad7c-01aa75ed71a1/language-en/format-PDF.
  • 7.Beaber EF, Sprague BL, Tosteson ANA, Haas JS, Onega T, Schapira MM, et al. Multilevel Predictors of Continued Adherence to Breast Cancer Screening Among Women Ages 50–74 Years in a Screening Population. J Womens Health 2002. 2019;28(8):1051–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Damiani G, Basso D, Acampora A, Bianchi CBNA, Silvestrini G, Frisicale EM, et al. The impact of level of education on adherence to breast and cervical cancer screening: Evidence from a systematic review and meta-analysis. Prev Med. 2015. Dec;81:281–9. doi: 10.1016/j.ypmed.2015.09.011 [DOI] [PubMed] [Google Scholar]
  • 9.Gathirua-Mwangi W, Cohee A, Tarver WL, Marley A, Biederman E, Stump T, et al. Factors Associated with Adherence to Mammography Screening Among Insured Women Differ by Income Levels. Womens Health Issues Off Publ Jacobs Inst Womens Health. 2018. Oct;28(5):462–9. doi: 10.1016/j.whi.2018.06.001 [DOI] [PubMed] [Google Scholar]
  • 10.Jensen LF, Pedersen AF, Andersen B, Vedsted P. Self-assessed health, perceived stress and non-participation in breast cancer screening: A Danish cohort study. Prev Med. 2015. Dec;81:392–8. doi: 10.1016/j.ypmed.2015.10.004 [DOI] [PubMed] [Google Scholar]
  • 11.Jensen LF, Pedersen AF, Andersen B, Vedsted P. Social support and non-participation in breast cancer screening: a Danish cohort study. J Public Health Oxf Engl. 2016;38(2):335–42. doi: 10.1093/pubmed/fdv051 [DOI] [PubMed] [Google Scholar]
  • 12.Melvin CL, Jefferson MS, Rice LJ, Cartmell KB, Halbert CH. Predictors of Participation in Mammography Screening among Non-Hispanic Black, Non-Hispanic White, and Hispanic Women. Front Public Health. 2016;4:188. doi: 10.3389/fpubh.2016.00188 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Schoofs J, Krijger K, Vandevoorde J, Devroey D. Health-related Factors Associated with Adherence to Breast Cancer Screening. J -Life Health. 2017. Jun;8(2):63–9. doi: 10.4103/jmh.JMH_71_15 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Volesky KD, Villeneuve PJ. Examining screening mammography participation among women aged 40 to 74. Can Fam Physician Med Fam Can. 2017. Jun;63(6):e300–9. [PMC free article] [PubMed] [Google Scholar]
  • 15.von Euler-Chelpin M, Olsen AH, Njor S, Vejborg I, Schwartz W, Lynge E. Socio-demographic determinants of participation in mammography screening. Int J Cancer. 2008. Jan 15;122(2):418–23. doi: 10.1002/ijc.23089 [DOI] [PubMed] [Google Scholar]
  • 16.Kriaucioniene V, Petkeviciene J. Predictors and Trend in Attendance for Breast Cancer Screening in Lithuania, 2006–2014. Int J Environ Res Public Health. 2019. 16;16(22). doi: 10.3390/ijerph16224535 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Zamorano-Leon JJ, López-de-Andres A, Álvarez-González A, Astasio-Arbiza P, López-Farré AJ, de-Miguel-Diez J, et al. Reduction from 2011 to 2017 in adherence to breast cancer screening and non-improvement in the uptake of cervical cancer screening among women living in Spain. Maturitas. 2020. May;135:27–33. doi: 10.1016/j.maturitas.2020.02.007 [DOI] [PubMed] [Google Scholar]
  • 18.Confidence Interval of a Proportion [Internet]. [cited 2020 Jun 23]. http://vassarstats.net/prop1.html.
  • 19.Joinpoint Regression Program, Version 4.8.0.1 –April 2020; Statistical Methodology and Applications Branch, Surveillance Research Program, National Cancer Institute.
  • 20.Andersen SB, Törnberg S, Kilpeläinen S, Lynge E, Njor SH, Von Euler-Chelpin M. Measuring the burden of interval cancers in long-standing screening mammography programmes. Journal of Medical Screening. 2015;22(2):83–92. doi: 10.1177/0969141314560386 [DOI] [PubMed] [Google Scholar]
  • 21.Gianino MM, Lenzi J, Bonaudo M, Fantini MP, Siliquini R, Ricciardi W, et al. Organized screening programmes for breast and cervical cancer in 17 EU countries: trajectories of attendance rates. BMC Public Health. 2018. Nov 6;18(1):1236. doi: 10.1186/s12889-018-6155-5 [DOI] [PMC free article] [PubMed] [Google Scholar]

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18 Jul 2022

PONE-D-21-29044Participation and adherence to mammography screening in the Capital Region of Denmark: The importance of age over timePLOS ONE

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Reviewer #1: The article deals with a very important issue. The manuscript seems technically sound to me, and the statistical analysis was performed appropriately and rigorously. The manuscript is well-written, with the exception of a couple of places where the authors used present tense when past tense was called for. The results are presented clearly in an orderly fashion and include a very informative and clearly presented table. The authors make some good points in the discussion and appropriately compare their results to those of many other studies. However, I am not clear regarding one of their attempts to explain why the most significant change occurred within the older age groups who participated to a larger extent than they did before, that being since the women aged by approximately 10 years during the study period, the higher participation is coherent with their slightly higher participation rate as younger women. I would have liked to see this idea fleshed out a little more. I agree with the authors' suggestion that personalized mammography screening utilizing risk-based screening recommendations could provide a better alternative to one-size-fits-all mammography screening programs. The authors did a good job in delineating possible limitations and a possible strength of the study. Finally, I don't see from the results the authors' statement in the conclusion that adherence was lower than the recommended 70%.

Reviewer #2: Thank you for asking me to review this manuscript.

Breast cancer is one of the most common cancer among women and important cause of death. Detection in early stage is curable and this is one of the cancers that can be screen detected. However, screening also leads to increase number of minor biopsy cases in BIRADS IV category. Voluntary participation is an important factor and adherence to screening program helps in reducing cancer mortality, this makes it an important manuscript.

I have a few observations to make

1. Authors state that this is analysis of registry data, according to me even this requires approval of the ethics committee, as authors state that Danish law does not require the approval, in that case it’s the ethical committee which should issue the waiver.

2. This is a longitudinal data over 20 year period, which is divided in 5 year age groups, during the 20 year period the participant would have moved from first group to nearly the last group, how is the movement of individual participant from one age group to other over subsequent years handled in the study?

3. Number of women participated in the program be separated from number of mammograms, as the mammograms will be repeated over period of time while number of eligible women will increase by addition of newer women becoming eligible.

4. Each women should be treated as a single case even if she underwent screening 10 times, this has not happened in this paper as all women in each round are counted this would mean a person may have been counted 10 times in 20 year period, the data should be separated.

5. There is no description of eligible population even number of women eligible at a point and overall (eligible in first year +added in second/third etc.)

6. It is not clear that the participation rates are for all eligible women or all women invited, authors should provide denominator and numerator beside percentage that is provided in text, it is important to mention how many women were eligible at a particular time

7. Has the reason for not participating recorded? Was invitation sent only once or was repeated?

8. Were any breast cancer awareness program or educational programs conducted between the study period? Were there any efforts to disseminate the importance of breast cancer screening and mammography? if so, could the increase be because of increase awareness

9. Did this increased participation resulted in increased detection (change in incidence)? Or stage shift?

10. Did this increased participation also resulted in increased rate of biopsies?

11. Most importantly did the mortality from breast cancer reduced as a result of increased participation in mammography screening?

12. What was the benefit of the program and increased participation rate that this article shows?

13. Though this study make us understand the age as important factor for participation in program, it does not inform what is the importance of this observation and also the remedies that may improve participation of younger women in breast cancer screening program (or no importance)

14. It is suggested that authors look at additional data and come out with newer findings (or benefits as sought above) that can help in improving the program and reducing the mortality from breast cancer, in its present form, the information provided in the manuscript is already known.

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Reviewer #1: No

Reviewer #2: No

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PLoS One. 2023 Jan 23;18(1):e0280790. doi: 10.1371/journal.pone.0280790.r002

Author response to Decision Letter 0


2 Oct 2022

We thank the reviewers for their comments to our manuscript and you will find our answers below.

Have the authors made all data underlying the findings in their manuscript fully available?

Answer: We have added the following statements to the Method section:

Data from this study are stored in Statistics Denmark, which only can be accessed given the relevant data permits in accordance with GDPR and Danish Law. The data is based on personal identification numbers and open access would seriously compromise the privacy of the women included in the study.

Reviewer #1:

However, I am not clear regarding one of their attempts to explain why the most significant change occurred within the older age groups who participated to a larger extent than they did before, that being since the women aged by approximately 10 years during the study period, the higher participation is coherent with their slightly higher participation rate as younger women.

Answer: Thank you for that comment and we agree that this is very unclear and we have rewritten the text as follows:

“Women in the youngest age group had over time an increased participation, which possibly influenced their adherence as they aged and moved into older age groups.”

I don't see from the results the authors' statement in the conclusion that adherence was lower than the recommended 70%.

Answer: This is indicated in Table 2 in the Results. However to make it clearer we have changed the sentence in Conclusion as follows:

“Complete adherence was lower than the recommended 70%, …”

Reviewer #2:

1. Authors state that this is analysis of registry data, according to me even this requires approval of the ethics committee, as authors state that Danish law does not require the approval, in that case it’s the ethical committee which should issue the waiver.

Answer: We have been informed that the statement we have provided in the manuscript regarding the need for ethics approval and/or review by a data protection committee satisfies the journal’s policies for research involving human participants.

2. This is a longitudinal data over 20 year period, which is divided in 5 year age groups, during the 20 year period the participant would have moved from first group to nearly the last group, how is the movement of individual participant from one age group to other over subsequent years handled in the study?

Answer: Thank you for this comment. This is longitudinal data over a 10 year period and the women will thereby have moved 1 to 2 age groups over the study period. They will have been screened a maximum of 5 times. Our aim was to assess adherence over time by age group which necessitates that women are included each time they are screened and not as a single case. We hope that the reviewer can accept this explanation.

3. Number of women participated in the program be separated from number of mammograms, as the mammograms will be repeated over period of time while number of eligible women will increase by addition of newer women becoming eligible.

Answer: Please see the explanation under point 2.

4. Each women should be treated as a single case even if she underwent screening 10 times, this has not happened in this paper as all women in each round are counted this would mean a person may have been counted 10 times in 20 year period, the data should be separated.

Answer: Please see the explanation under point 2.

5. There is no description of eligible population even number of women eligible at a point and overall (eligible in first year +added in second/third etc.)

Answer: In Table 1 the absolute number of invited women and participating women are given for each age group and each invitation round. In view of our aim to assess adherence, we hope this answer is acceptable to the reviewer.

6. It is not clear that the participation rates are for all eligible women or all women invited, authors should provide denominator and numerator beside percentage that is provided in text, it is important to mention how many women were eligible at a particular time

Answer: Please see under point 5.

7. Has the reason for not participating recorded? Was invitation sent only once or was repeated?

Answer: We have not recorded the reason for not attending in this study. We have added information regarding reminders as follows:

“Women who do not show up are sent a reminder.”

8. Were any breast cancer awareness program or educational programs conducted between the study period? Were there any efforts to disseminate the importance of breast cancer screening and mammography? if so, could the increase be because of increase awareness.

In Denmark all women aged 50-69 are individually invited biennially to screening with mammography. At that time they receive information about advantages and risks with screening in order for them to make an informed choice of whether to participate or not. No regional or national campaigns have existed in the study period.

9. Did this increased participation resulted in increased detection (change in incidence)? Or stage shift?

Answer: To assess the detection rate is beyond the scope of this study, as our aim was to assess adherence to the program over time by age group.

10. Did this increased participation also resulted in increased rate of biopsies?

Answer: Please see the answer above.

11. Most importantly did the mortality from breast cancer reduced as a result of increased participation in mammography screening?

Answer: Certainly the aim with screening is to lower the mortality from breast cancer in the population, but mortality rate is a long time measure, so in the meantime we use short time indicators, out of which one is to study participation and adherence, see European guidelines for quality assurance in breast cancer screening and diagnosis.

12. What was the benefit of the program and increased participation rate that this article shows?

Answer: The study points to the change of age as being a stratifying factor for participation to a more equal participation in all age groups, and thereby suggests that other factors might be more determining, and more personalized screening might be beneficial.

13. Though this study make us understand the age as important factor for participation in program, it does not inform what is the importance of this observation and also the remedies that may improve participation of younger women in breast cancer screening program (or no importance)

Answer: In Denmark there is no recommendation that women younger than 50 should be offered screening. Within the youngest age group are the first time invitees and therefore there are a certain group that will opt out of the program and will not be invited further. This is explained in the first paragraph of the Discussion.

14. It is suggested that authors look at additional data and come out with newer findings (or benefits as sought above) that can help in improving the program and reducing the mortality from breast cancer, in its present form, the information provided in the manuscript is already known.

Answer: We thank the reviewer for this comment and more research is certainly ongoing

Attachment

Submitted filename: Response to the reviewers.docx

Decision Letter 1

Sandar Tin Tin

10 Jan 2023

Participation and adherence to mammography screening in the Capital Region of Denmark: The importance of age over time

PONE-D-21-29044R1

Dear Dr. Pett,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Sandar Tin Tin

Academic Editor

PLOS ONE

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: (No Response)

Reviewer #3: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #2: Yes

Reviewer #3: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: I Don't Know

Reviewer #3: Yes

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4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #2: No

Reviewer #3: (No Response)

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #2: Yes

Reviewer #3: (No Response)

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2: I thank authors for their response however, the response to some of the questions is not satisfactory like that of Q2,3, and 4

I do not see any modifications made in the manuscript as per comments

Reviewer #3: All comments from reviewers have been addressed appropriately. It is now acceptable for publication.

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: No

Reviewer #3: Yes: Rasmi G. Nair

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Acceptance letter

Sandar Tin Tin

13 Jan 2023

PONE-D-21-29044R1

Participation and adherence to mammography screening in the Capital Region of Denmark: The importance of age over time

Dear Dr. Pett:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Sandar Tin Tin

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    Attachment

    Submitted filename: Response to the reviewers.docx

    Data Availability Statement

    The data underlying this article cannot be shared for the privacy of the individuals who participated in the mammography screening programs. The data will be shared on reasonable request to the corresponding author. The data are stored in the national bureau of statistics in Denmark, called Statistics Denmark (DST). The data is pseudo-identified, i.e. the Danish personal identification number is switched with another number. However, there is a key between the two which according to Danish law constitutes a risk for potential identification. The data can, with the relevant permissions, be accessed by contacting the Department of Public Health, University of Copenhagen, Denmark with reference to the research project “Benefits and harms of screening for breast cancer with mammography” and through that department potentially gain access to the data at DST. Department of Public Health Faculty of Health and Medical Sciences University of Copenhagen Phone: +45 35 32 76 23 Department contact: George Napolitano, gena@sund.ku.dk https://publichealth.ku.dk/.


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