for mammography screening to reduce breast cancer mortality , a large proportion of the targeted women must be screened . monitoring recruitment and quality indicators for mammography screening are specified in the european guidelines for quality assurance in breast cancer screening and diagnosis , and these include monitoring the coverage of the targeted population by invitation to screening , the coverage of the targeted population by screening examination , and the participation rate in screening among invited women . a survey of european mammography screening programmes showed that coverage by examination varied from about 30% to about 90% , indicating large differences in the potential impact of screening on breast cancer mortality . low coverage by examination in an organized programme may reflect that some targeted women attend opportunistic screening or it may reflect low acceptability of screening . the organizational aspects of the programme very probably also play a role . we evaluated the effect of variations in the invitation scheme on coverage and participation through more than 20 years of the organized , population - based mammography screening programme in copenhagen , denmark . organized , population - based mammography screening in the copenhagen municipality started on 4th april 1991 . the target population was women aged 5069 residing in the municipality of copenhagen , identified via the daily updated danish civil registration system ( crs ) . over time , various small subgroups were considered ineligible for screening ( see below ) . invitation rounds were of approximately two years ( appendix table 2 ) . invited women received a personal letter with a fixed , changeable date of appointment . women born in january were invited during the first two months of the first year of an invitation round , women born in february were invited during the next two months , etc . initially , women already diagnosed with breast cancer and known in the register of the danish collaborative breast cancer group were considered ineligible and excluded from invitation , but this stopped as it became clear that the register was not sufficiently updated for this purpose . over time , exclusions encompassed some women with breast cancer , some with bilateral mastectomy , and some with breast prostheses prohibiting the mammography examination . later , women with breast cancer surgery more than 18 months ago were again invited for screening . from the beginning , a woman could notify the clinic if she did not want to be invited again , in which case she did not receive any further invitation ( appendix table 3 ) . 
  in invitation rounds 17 , women aged 5069 at the start of each round were invited ( figure 1 ) . in invitation all women were invited to the next round , except those who had notified the programme not to be re - invited , moved out of the area , or passed the upper age limit for re - invitation . in invitation rounds 6 and 7 , approximately 10% of the target population were not invited due to unidentified technical errors in the invitation system . figure 1.cohorts of women first targeted by the copenhagen programme at age 5051 by age , invitation rounds , and invitation numbers ( marked in graph ) . cohorts of women first targeted by the copenhagen programme at age 5051 by age , invitation rounds , and invitation numbers ( marked in graph ) . from invitation round 8 onwards , invitations were planned to be issued according to attained age , meaning that women aged 5069 at the invitation date were invited to screening . women received the first invitation at age 5051 and the last at age 6869 , depending on age at first invitation . exceptionally for round 8 , invitations included all women from the age of 48 at the start of round 8 . for invitation round 8 , part of non - participants from round 7 , including those not invited due to technical errors , were not invited . women previously administratively excluded due to technical errors were re - invited in invitation round 9 . however , in invitation rounds 9 and 10 , women who had not responded to the previous two invitation rounds ( previous passive non - participants ) were not invited . crs holds information on current and historical addresses for residents in denmark since 1968 . from the crs , we identified the target population of the copenhagen municipality screening programme from 1 april 1991 to 12 july 2012 , covering 10 biennial invitation rounds . from invitation rounds 18 , the copenhagen screening programme kept a mammography register with the personal identification number ( including information on and date of birth ) , date of invitation , dates of reminders , date of screening , outcome of screening , and ( where relevant ) dates and outcome of assessment and surgery . the register also included information on women who had notified the programme that they did not want to be invited , and the register included codes for ineligibility . from invitation round 9 onwards , the copenhagen programme became incorporated into the larger programme for the capital region of denmark . the structure of the mammography screening register for the capital region differs from the old register from copenhagen . however , it is possible from this new register to obtain the same information as before , apart from ineligibility , for which only the latest registration was kept in the new register . we linked the data retrieved from the crs and the screening registers , which provided us with a complete invitation history of all targeted women . to control for age and number of offered screens when we compared coverage with participation , we constructed nine closed cohorts , each including women aged 5051 at the start of their first invitation round ( cohort 19 ) . these cohorts were followed up from the first through subsequent invitation rounds ( 110 , 19 , 12 ) , each time including those present from the cohort at the start of a given round . each cohort was tabulated by number of women targeted , number of women invited , and number of women participating by invitation round and invitation number . we were not able to tabulate the number of eligible women for invitation rounds 910 , as only the latest ineligibility code was kept in the system . we also calculated coverage by invitation ( number of invited women divided by number of women in the target population ) , coverage by examination ( number of participating women divided by number of women in the target population ) , and participation rate ( number of participating women divided by number of invited women ) by invitation round and invitation number . the change in invitation scheme in round 8 to include all women from age 48 onwards meant that our cohort 9 started with the second invitation number . organized , population - based mammography screening in the copenhagen municipality started on 4th april 1991 . the target population was women aged 5069 residing in the municipality of copenhagen , identified via the daily updated danish civil registration system ( crs ) . over time , various small subgroups were considered ineligible for screening ( see below ) . invitation rounds were of approximately two years ( appendix table 2 ) . invited women received a personal letter with a fixed , changeable date of appointment . women born in january were invited during the first two months of the first year of an invitation round , women born in february were invited during the next two months , etc . initially , women already diagnosed with breast cancer and known in the register of the danish collaborative breast cancer group were considered ineligible and excluded from invitation , but this stopped as it became clear that the register was not sufficiently updated for this purpose . over time , exclusions encompassed some women with breast cancer , some with bilateral mastectomy , and some with breast prostheses prohibiting the mammography examination . later , women with breast cancer surgery more than 18 months ago were again invited for screening . from the beginning , a woman could notify the clinic if she did not want to be invited again , in which case she did not receive any further invitation ( appendix table 3 ) . 
  in invitation rounds 17 , women aged 5069 at the start of each round were invited ( figure 1 ) . in invitation all women were invited to the next round , except those who had notified the programme not to be re - invited , moved out of the area , or passed the upper age limit for re - invitation . in invitation rounds 6 and 7 , approximately 10% of the target population were not invited due to unidentified technical errors in the invitation system . figure 1.cohorts of women first targeted by the copenhagen programme at age 5051 by age , invitation rounds , and invitation numbers ( marked in graph ) . cohorts of women first targeted by the copenhagen programme at age 5051 by age , invitation rounds , and invitation numbers ( marked in graph ) . from invitation round 8 onwards , invitations were planned to be issued according to attained age , meaning that women aged 5069 at the invitation date were invited to screening . women received the first invitation at age 5051 and the last at age 6869 , depending on age at first invitation . exceptionally for round 8 , invitations included all women from the age of 48 at the start of round 8 . for invitation round 8 , part of non - participants from round 7 , including those not invited due to technical errors , were not invited . women previously administratively excluded due to technical errors were re - invited in invitation round 9 . however , in invitation rounds 9 and 10 , women who had not responded to the previous two invitation rounds ( previous passive non - participants ) were not invited . crs holds information on current and historical addresses for residents in denmark since 1968 . from the crs , we identified the target population of the copenhagen municipality screening programme from 1 april 1991 to 12 july 2012 , covering 10 biennial invitation rounds . from invitation rounds 18 , the copenhagen screening programme kept a mammography register with the personal identification number ( including information on and date of birth ) , date of invitation , dates of reminders , date of screening , outcome of screening , and ( where relevant ) dates and outcome of assessment and surgery . the register also included information on women who had notified the programme that they did not want to be invited , and the register included codes for ineligibility . from invitation round 9 onwards , the copenhagen programme became incorporated into the larger programme for the capital region of denmark . the structure of the mammography screening register for the capital region differs from the old register from copenhagen . however , it is possible from this new register to obtain the same information as before , apart from ineligibility , for which only the latest registration was kept in the new register . we linked the data retrieved from the crs and the screening registers , which provided us with a complete invitation history of all targeted women . to control for age and number of offered screens when we compared coverage with participation , we constructed nine closed cohorts , each including women aged 5051 at the start of their first invitation round ( cohort 19 ) . these cohorts were followed up from the first through subsequent invitation rounds ( 110 , 19 , 12 ) , each time including those present from the cohort at the start of a given round . each cohort was tabulated by number of women targeted , number of women invited , and number of women participating by invitation round and invitation number . we were not able to tabulate the number of eligible women for invitation rounds 910 , as only the latest ineligibility code was kept in the system . we also calculated coverage by invitation ( number of invited women divided by number of women in the target population ) , coverage by examination ( number of participating women divided by number of women in the target population ) , and participation rate ( number of participating women divided by number of invited women ) by invitation round and invitation number . the change in invitation scheme in round 8 to include all women from age 48 onwards meant that our cohort 9 started with the second invitation number . our study included 47,990 screen targeted women , of whom 45,597 were invited ; of these , 31,424 participated in screening ( appendix table 4 ) . coverage by invitation for the newly recruited cohorts of women aged 5051 was close to 95% in all invitation rounds except round 2 , where it reached 99.5% , and round 7 where it dropped to 93.7% ( table 1 ) . for cohort 1 , coverage by invitation dropped gradually over successive invitation numbers , from 95.6% at first invitation to 87.4% at fifth invitation . a dramatic drop to 70.0% at invitation 6 was observed , remaining low at invitations 7 and 8 and then increasing again to 76.6% at invitation 9 . similar changes were seen for cohort 2 at invitations 5 and 8 , respectively , and for cohort 3 at invitations 4 and 7 , respectively , and so forth for successive cohorts . these dramatic drops in coverage by invitation reflected the errors in the invitation scheme in invitation rounds 68 , and the equally dramatic increases reflected the deletion of previous administrative exclusions in invitation round 9 . the low number for cohort 1 invitation 10 ( 17.1% ) reflected that women were no longer invited when they turned 70 . table 1.coverage by invitation ( % ) , coverage by participation ( % ) , and participation rates ( % ) by invitation rounds and invitation numbers for women first targeted by the copenhagen screening programme at age 5051.invitation round , first targeted  =  cohort numberinvitation number12345678910coverage by invitation ( % ) 195.693.790.488.387.470.068.067.876.617.1299.591.889.488.568.967.768.080.078.1395.993.592.372.270.069.182.079.0495.693.478.176.374.678.976.6594.992.889.784.870.868.4696.091.790.972.370.7793.791.775.372.6895.491.088.59nr89.287.1coverage by examination ( % ) 172.566.065.663.961.759.356.656.552.411.1270.464.162.960.057.457.157.557.354.5366.563.560.758.857.657.859.057.4467.162.360.759.860.860.958.0563.961.462.563.259.656.6662.763.063.860.858.5763.062.159.957.9864.263.159.19nr60.658.9participation rate ( % ) 175.970.472.572.370.684.883.383.468.464.9270.769.970.367.683.384.384.671.669.8369.367.965.781.482.383.672.072.7470.266.777.778.481.677.175.7567.466.169.774.584.282.9665.368.770.284.182.8767.267.879.679.8867.269.366.89nr68.468.0 : invitation round 15 . coverage by invitation ( % ) , coverage by participation ( % ) , and participation rates ( % ) by invitation rounds and invitation numbers for women first targeted by the copenhagen screening programme at age 5051 . : invitation round 15 . coverage by examination for the newly recruited women was 72.5% for cohort 1 , but dropped below 70% for cohort 3 onwards , and was 64.2% for cohort 8 . for cohorts 14 , coverage by examination dropped by increasing invitation number , for cohort 1 from 72.5% at invitation 1 to 52.4% at invitation 9 ( table 1 and figure 2 ) . cohorts 58 started out with a lower coverage by examination ( around 63% ) than the previous cohorts , but tended to maintain this level through the next 34 invitations . these changes did not clearly affect the coverage by examination in the earliest cohorts , probably because these old cohorts would have accumulated many technical errors , and the deletion of these errors would tend to increase coverage by examination , and because the omitting to invite those not attending the last two times would tend to decrease coverage by examination . however , in cohorts 58 , where less technical errors were accumulated , omitting to invite women not attending the last two times clearly resulted in a decrease in coverage by examination , e.g. from 63.8 to 60.8%/58.5% in cohort 6 . in cohort 8 , this change would be expected only in invitation 3 , which was also the case . figure 2.average coverage by examination ( % ) for cohorts of women first targeted by the copenhagen programme age 5051 by invitation number and invitation round . average coverage by examination ( % ) for cohorts of women first targeted by the copenhagen programme age 5051 by invitation number and invitation round . participation rate at first invitation number was 75.9% for cohort 1 , but dropped below 70% from cohort 5 onwards , reaching 67.2% for cohort 8 ( table 1 ) . for cohort 1 , the dramatic changes in coverage by invitation across invitation number were reflected in opposite dramatic changes in the participation rate , increasing from 70.6% at invitation 5 to 84.8% at invitation 6 and then dropping again to 68.4% at invitation 9 . similar patterns were seen for the other cohorts . while the changes due to the errors in the invitation scheme during invitation rounds 68 became less visible in the participation rates for the later cohorts , the drop in coverage by invitation during invitations rounds 9 and 10 the figure clearly shows the gap that developed between the two measures after invitation 5 . figure 3.coverage by examination ( % ) and participation rate ( % ) for cohorts of women first targeted by the copenhagen programme age 5051 by invitation number . coverage by examination ( % ) and participation rate ( % ) for cohorts of women first targeted by the copenhagen programme age 5051 by invitation number . this study demonstrates the impact of the invitation scheme on the european union quality indicators for mammography screening . first , the participation rate in an organized mammography screening programme seemed highly dependent on the invitation scheme , with about a 20% increase ( e.g. invitation 4 from 67.6 to 84.1%/79.8% ) when invitations were restricted to those who participated in the previous round . second , coverage by examination seemed to decrease by between 8 and 16% with increasing invitation number over seven invitation rounds ( e.g. cohort 4 from 67.1 to 58.0% ) . third , for the latest recruited cohorts the coverage by examination tended to drop by 510% when non - attenders from the previous round were not re - invited ( e.g. cohort 6 from 63.8 to 60.8%/58.5% ) . this change was less visible in the earlier recruited cohorts , where it was balanced out by simultaneous deletion of old technical errors . fourth , over time the participation rate became an increasingly bad indicator of coverage by examination ( e.g. cohort 1 showing a gap from 68.4 to 52.4% at invitation 9 ) . because the crs tracks all residents in denmark , we could on each starting date of an invitation round identify the closed cohort of women aged 5051 and living in the municipality of copenhagen . linkage between crs and screening registers was based on the unique personal identification numbers , so we could accurately identify the target population , the invited women , and the participating women . many studies have documented the impact of the information approach on the participation in screening . it is a further strength of our study that throughout the entire study period , invited women received a personal invitation letter with a fixed , changeable date of appointment . a limitation in the study was that because the latest ineligibility code was not kept in the system for invitation rounds 910 , it was not possible to separate out the impact of changes in ineligibility criteria from the impact of errors in the invitation data . however , the only quantitatively important change in ineligibility was probably the increase in coverage by invitation from 95.6% in invitation round 1 to 99.5% in invitation round 2 , when the linkage with the register of the danish breast cancer cooperative group stopped . in invitations rounds 17 , some women could be 53 before their first invitation . for that reason , in invitation rounds 810 women turning 50 before their birth cohort had been invited were invited in the current round . in invitation round 10 , those turning 70 during the round were invited in total only nine times . to take account of this , from invitation round 11 onwards , it might be expected that a high coverage by invitation would be associated with a low participation rate , however such an association could not be found in the survey data from 25 european screening programmes . both coverage by invitation and participation rate can be affected by local factors , complicating comparison across european countries . for mammography screening to decrease breast cancer mortality in the targeted population , coverage by examination breast cancer mortality in the target population of the copenhagen programme decreased by 25% during the first 10 years after the programme started . these results derived from the early recruited cohorts starting out with a coverage by examination of 6773% . however , the cohorts recruited later started out with a coverage by examination of 6364% , a drop expected to have an impact on the outcome of screening at the population level . during the first 10 years of the copenhagen programme , breast cancer mortality in screened women dropped by 37% , and this effect is expected to be seen also in screened women from later recruited cohorts . the slight drop in coverage by examination following the cessation of re - invitation of non - attenders was seen for the later , but not the earlier cohorts , probably due to the coinciding deletions of technical errors . the drop is a matter of concern , especially because the later cohorts already had a lower coverage by examination at first invitation than previous cohorts . in 2015 , the copenhagen programme went back to the previous procedure and now re - invites all women except those who actively opted out . we will thus never get long - term data from copenhagen on the impact of the limited invitation scheme . nevertheless , our data can serve as a warning for other programmes that for logistical reasons want to limit invitations to previous attenders . the european guidelines use coverage by invitation , coverage by examination , and participation rate as quality indicators , but acceptable and desirable levels of achievement are given only for the participation rate ( 70 and 75% , respectively ) . there are good reasons for this limitation , as the participation rate can normally be calculated from the screening programme data alone , while the two other measures require access to accurate and updated population data . our study nevertheless demonstrated that the participation rate can be considerably higher than the coverage by examination . unless limitations in the invitation scheme are taken into account , health authorities focusing on the participation rate may expect their target population to be better protected against death from breast cancer by a screening programme than is actually the case . our study demonstrates the complexity of measuring even simple quality indicators , such as coverage by invitation , coverage by examination , and participation rate . part of this complexity may be derived from errors in the invitation scheme in the copenhagen programme , but denmark has better population registers than almost all other screening settings , and it is unlikely that errors such as those in the copenhagen programme would not also occur in other programmes . the difference may be that the quality of the danish registers allowed the impact of such errors to be documented . our study demonstrates that coverage by examination tended to decrease over successive rounds of a mammography screening programme . the participation rate was highly sensitive to changes in the invitation scheme , increasing considerably when previous non - attenders were not re - invited . we observed a considerable gap between the coverage of examination and the participation rate , strongly indicating that the latter can not , without reservations , be taken as an indicator of the former . health care administrators should be aware of this interplay between the quality indicators , in order to avoid that interpretation that the participation rate is a direct reflection of the coverage by examination . the author(s ) declared no potential conflicts of interest with respect to the research , authorship , and/or publication of this article . the author(s ) received no financial support for the research , authorship , and/or publication of this article .
backgroundthe purpose of mammography screening is to decrease breast cancer mortality . to achieve this a high coverage by examination 
 is needed . within an organized screening programme 
 , we examined the impact of changes in the invitation schedule on the interplay between coverage and participation.methodwe studied nine cohorts aged 5051 when first targeted by mammography screening in copenhagen , denmark . 
 population data were retrieved from the danish civil registration system ; invitation and attendance data from the screening programme database . 
 data were linked using unique personal identification numbers . 
 coverage by invitation was defined as ( number of invited women / number of targeted women ) , coverage by examination as ( number of screened women / number of targeted women ) , and participation rate as ( number of screened women / number of invited women).resultscoverage by invitation was close to or above 95% for all newly recruited cohorts . in subsequent invitation rounds , both technical errors and changes in the invitation scheme affected the coverage by invitation . 
 coverage by examination at first invitation was 72.5% for the first cohort , but dropped to 64.2% for the latest cohort 
 . furthermore , coverage by examination dropped by increasing invitation number and with omission of re - invitation of previous non - attenders . 
 participation rate closely reflected changes in the invitation scheme.conclusionchanges in the invitation schemes influenced coverage by invitation , coverage by examination , and participation rate . 
 we observed a considerable gap between coverage by examination and participation rate , strongly indicating that the latter can not without reservations , be taken as an indicator of the first .