Flemish breast cancer screening programme: 15 years of key performance indicators (2002–2016)

Breast cancer (BC) is a leading cause of disease burden among women in Europe: an estimated 522,513 women were diagnosed with BC in 2018, and 137,707 died of BC that year (GLOBOCAN 2018). Mammographic screening can reduce BC mortality in women over 50 years old, although the magnitude of this mortality reduction is the subject of ongoing debate. Estimates range from 20% or less for the group invited to screening, to 48% for the group that gets screened [1, 2]. Mammographic screening also has limitations, including the occurrence of interval cancers and diagnosing BC that never would have been diagnosed nor caused symptoms in the absence of screening (overdiagnosis).

Many countries offer mammographic screening in the framework of a population-based mammography screening programme (PMSP), which aims to give all asymptomatic women in the target population systematic and equal access to screening while quality assurance and data collection are performed in a centralized manner. A PMSP can exist in parallel with opportunistic screening, which follows the spontaneous initiative of the woman or her physician [3].

Using breast cancer mortality as an endpoint in the evaluation of a PMSP seems obvious, but it takes many years before an effect on mortality can be observed [4]. Key performance indicators (KPIs) cannot replace a mortality analysis, but enable programmes to compare performance against objectives. Monitoring and evaluating KPIs (such as cancer detection rate or programme sensitivity) is a necessity for public health interventions such as a PMSP to justify the use of public means [1, 4].

We calculated KPIs for the Flemish PMSP for the years 2002–2016, benchmarked crude KPI results against KPI-targets set by the European guidelines and KPI results of other national screening programmes, and examined temporal trends in age-standardised KPIs.

Table 1 shows that between 2002 and 2016, a total of 2,613,737 PMSP screenings were performed, of which a BCR link was established for 97.7%. These women had a mean age of 58.6 (years).

We analysed key performance indicators for the Flemish PMSP for the period 2002–2016.

A much larger fraction of the population was covered in 2016 (64.2%) compared to the start of the programme (46.2% in 2003), even though the response to the screening invitation remained stable throughout 15 years. The growth in coverage slowed down after the majority of women started receiving timely invitations (93.2% in 2011). This indicates that the PMSP coverage increase was not so much the result of a change in intention to screen among the target group, but was instead largely due to the fact that more women were receiving their invitation on time.

Opportunistic screening was well established in Belgium long before the PMSP started [12]. Between 2003 and 2016, opportunistic coverage gradually decreased (AAPC −3.0%). Many of these women gradually switched to the PMSP. Several factors may have encouraged this switch: the quality of the opportunistic screening is not guaranteed (quality assurance of equipment, double-reading, etc.), opportunistic screening is not entirely free of charge, and booking appointments for a PMSP screening requires less effort from the women. Nevertheless, 14.1% of women preferred opportunistic screening in 2016. Previous studies indicate that physician’s advice is the primary reason for not switching [13].

The decrease in recall rate, combined with the stable CDR, means that fewer women are receiving a false-positive recall (20.2/1000 screens in 2016) leading to a higher positive predictive value of the screening mammograms (21.3% in 2016), which is also above the EU mean of 12.2% [3]. There are several hypotheses for this. Firstly, yearly symposia on lowering recall rate have been organized by the CvKO since 2010. Secondly, individual 4-monthly feedback is sent to all readers since 2008–2009. These reports compare their individual recall rate with the anonymised rates of their colleagues. Thirdly, the introduction of digital mammography screening, which led to an increased CDR in other countries [14], occurred in the same period as the reduction of the recall rate. Theoretically, the introduction of digital screening could have increased the CDR and thereby masked the lowering of CDR due to more restrictive recall strategy. However, this is unlikely as previous research has shown that digitalization in Flanders did not result in significantly different cancer detection rates [15]. Although the lowering of recall rate in combination with a stable CDR is a positive evolution, it is necessary to evaluate the negative counterpart i.e. interval cancer rate. More specifically, a review of interval cancers could determine whether breast cancers are more likely to be missed compared to other countries.

Surprisingly, the tumour stage distributions hardly differ between initial and subsequent regular screening. The same is true for CDR: in 2016 the CDR was 5.0‰ in subsequent regular screens (EU mean 5.6‰) and 6.3‰ in initial screens (EU mean 7.2‰) [3]. This could be explained by a large proportion of “initial screens” which were preceded by opportunistic screening [16]. In 2019, the CvKO will pilot a method that adjusts the KPIs of initial screens for the occurrence of such preceding opportunistic screening.

Benchmark targets for nodal status have not been achieved in 2015. This could be partly caused by the fact that more than 10% of 2015’s invasive SDC still have unknown nodal status. Assuming at least some of these unknown cases are node negative, the benchmark targets might be achieved.

Programme sensitivity is stable (65.1% in 2014) but lower than in other countries such as Germany (78.2%) [17], the Netherlands (74.4%) [18], Norway (75.5%) [19], or Canada (68%) [20]. Closer inspection reveals that the categorization of BC as either SDC or interval cancers differs between programmes. For instance, in the German programme any BC found within 24 months after a positive screening was considered an SDC, while the Canadian Programme only considered a BC as screen detected if they were found within 6 months after a positive screening [17, 20]. The Canadian programme will thus classify certain BC as interval cancers, while the German programme would see them as SDC. Such differences will influence programme sensitivity. The Flemish PMSP only considers a BC as screen detected if it was found within 3 months after the first diagnostic assessment that follows a positive screening (see also Table 2) [21]. The Canadian definition of an SDC is relatively close to the Flemish, which might explain why their programme sensitivity is similar (68% in Canada, 65.1% in Flanders) [20].

To decrease the risk of missing BC (thereby increasing sensitivity), the CvKO started a self-teaching project in 2018 which provides all readers with a yearly list of BC for which they had made a negative reading. To counter a possible increase in recall rate, readers also receive a list of their positive readings in which no breast cancer was found in the 2 years following screening.

The major strength of this first nationwide analysis of KPIs in the Flemish PMSP is the availability of national data on all mammographic PMSP screenings performed over 15 years, together with the matched oncological follow-up data from the BCR. The completeness of BCR breast cancer data was previously estimated to be 99.7% [6].

Our study also has some limitations. Firstly, not all screened women provided an informed consent to link their screening data to the BCR data, mostly during the programme initiation in 2002 and 2003. Refusal rates fluctuated around 1% or less of screened women. Secondly, we suspect that some of the “initial screens” in the programme are in fact preceded by opportunistic screen. We are investigating this further. Thirdly, some of the tumor characteristics have missing data, meaning the proportions calculated for those KPIs might still rise. For instance, in 2015 65.4% of invasive BC were node-negative, but a further 11.2% had unknown nodal status. The same is true for stage distribution. Fourthly, we considered all diagnostic mammograms as opportunistic screening, even though a minority are undoubtedly for diagnostic purposes [12]. The BCR and CvKO are currently investigating the proportion of all diagnostic mammograms that are for screening purposes. Fifthly, in the current analysis, we cannot estimate the impact on breast cancer mortality. The CvKO participates in the EU-topia project (https://​eu-topia.​org) to attempt to obtain an estimate, while the BCR is currently performing its own analysis.

Besides the suboptimal attendance rate, most performance indicators in the Flemish PMSP meet EU benchmark targets. Nonetheless, there are several priorities for further investigation. Firstly, the response to invitation has remained stable, indicating that the strategies that have been used to increase screening uptake these last 15 years have had limited effect. Now that the invitation scheme has been optimised, a critical evaluation should be made of these strategies. Secondly, interval cancers should be analysed by individual radiological review as described in the European guidelines [4]. If the proportion of “missed cancers” is comparable to the results in other countries, it can be concluded that Flanders has found a successful way of reducing recall rate while maintaining a stable CDR. The ensuing lower number of false positive screenings will lead to increased rescreening rates [22, 23]. Thirdly, ways must be found to further limit the occurrence of interval cancers after positive screenings with negative diagnostic assessment. One possibility could be to let diagnostic assessment only take place in specialised centres. Fourthly, the clinical and health economic impact of the PMSP should be analysed, along with the effect of opportunistic screening on CDR in initial and subsequent irregular screens. The BCR and CvKO are therefore analysing the impact of mammographic screening in three scenarios: women attending PMSP, women attending only opportunistic screening, women attending both screening types. Among other things, the study will compare cost-effectiveness and clinical outcome. This is being done in parallel with efforts to estimate the impact on breast cancer mortality.