Worldwide, breast cancer is the most common cause of cancer death in women (1). In 2018 the global age-standardized incidence and mortality rates of breast cancer were 54.4 and 11.6 per 100,000 women, respectively (1). Randomized controlled trials have confirmed that mammography screening can reduce the risk of breast cancer mortality by 20% for women aged 50–70 who attend this screening (2). The European guideline for quality assurance in breast cancer screening and diagnosis suggests to strive for 70% screening coverage in order to have a significant effect on breast cancer burden in the population. However, this percentage is not obtained in many countries where a breast cancer screening program (BCSP) has been established. In Europe, the mean screening coverage is about 50% (range 28–92%), meaning that a large proportion of women who are eligible for screening are not covered by the population breast cancer screening programs. This does not mean that these women do not receive any form of BC screening, since opportunistic BC screening exists in many countries (3).

To understand the reasons for this low coverage, several studies assessed the determinants of screening coverage. The main reported determinants of low screening coverage were related to low socioeconomic status (SES): lower income level, having an immigrant background, and being a single parent (4–7). The conclusions of these studies are mainly derived from linear regression modeling, in which the change in the mean coverage is estimated as a function of the explanatory variables. However, the determinants of the lowest and highest screening coverage are more of interest to policymakers than the determinants of the average coverage. In order to improve the screening coverage of BCSP, it is important to know the characteristics of the women with the lowest coverage in the BCSP, as well as those of the women with the highest coverage in the opportunistic screening. These insights can assist policy makers to implement specific actions to increase the screening coverage of BCSP, especially for those groups that are not covered by opportunistic screening either.

The aim of this study was therefore to evaluate the effect of socio-demographic factors and indicators for SES at the lower end of screening coverage in the BCSP and the higher end of opportunistic screening coverage. Data of screening coverage in Flanders, Belgium were analyzed with a quantile regression model (8).

We found that a larger percentage of foreign residents and a larger average household size as indicators for lower SES were found in neighborhoods with a lower coverage in the BCSP. However, a higher average personal annual income as an indicator for a higher SES was also found in neighborhoods with a lower coverage in the BCSP. For these neighborhoods, the negative association between SES and coverage in the BCSP was stronger than in the neighborhoods with a relatively middle SES level. The neighborhoods with a higher coverage of opportunistic screening had a relatively higher average personal annual income and the positive association between SES and coverage of the opportunistic screening was stronger than in neighborhoods with a relatively lower SES level.

The median coverage in the BCSP for all neighborhoods was 50%. The median coverage for neighborhoods in the lowest and the highest quantile was 33.5 and 64.5%, respectively. The coverage in the BCSP in Flanders was lower than in countries like the Netherlands and the United Kingdom where BC screening is mainly performed in the BCSP, but it was close to countries like France and Germany where both BCSP and opportunistic screening are performed for BC screening (17). As the median coverage of the opportunistic screening was 12%, with 4.2% coverage in the neighborhoods in the lowest quantile and 24.8% coverage in the neighborhoods in the highest quantile, the combined coverage in the BCSP and the opportunistic screening was relatively close to the BC screening coverage in other Western European countries (3, 17).

We observed that women in neighborhoods with a lower SES, as indicated by a crowded housing condition (18, 19) or being an immigrant with a foreign nationality (20), tended to participate less in the BCSP than women in neighborhoods with middle level SES. The negative association between these variables and the coverage in the BCSP was previously also found in other European countries (21, 22). An explanation for this phenomenon is that women with a relatively low SES have a possible lack of health literacy, leaving them less informed on the benefit of BCSP (23). Other reasons may include language barriers for women with an immigration background (24), and the fact that the hardship of life for women with relatively low SES may require more time to work than high SES women and reduce the attention to health care (25).

Interestingly, we also found that women in neighborhoods with a higher income as indicated by a higher average personal annual income also tend to participate less in the BCSP than the women in neighborhoods with middle level income. However, these women tend to participate more in the opportunistic screening than the women in neighborhoods with middle level income. Studies in France, where BCSP and opportunistic screening coexist as in Flanders, also found that women in the most affluent group tend to participate more in opportunistic screening (26). A possible explanation for this phenomenon is that women who belong to the neighborhoods with a relatively high SES may prefer the opportunistic screening which has a more flexible time schedule and more personalized service than the BCSP (2, 27).

The strength of this study is that the validity of the screening coverage data was warranted by the administrative database of the screening program in Flanders. The recall bias in self-reported surveys was avoided in our data (28). Moreover, the determinants of screening coverage were evaluated for the full distribution of the coverage in the BCSP and the opportunistic screening. The heterogeneous effect of the determinants of screening coverage in different quantiles can provide a more specific target for the potential interventions to improve the screening coverage rate. A limitation of this study was that all data were aggregated at a neighborhood level. It was therefore not possible to explore the variation within the neighborhoods due to the aggregated nature of the data. Moreover, the aggregated data in the current data do not contain factors that have a potential impact on the implementation of the screening, such as women's contract information with general practitioners which might play an important role in the implementation of opportunistic screening. However, studies have shown that residents who live in the same neighborhood share similar SES and health behavior (29, 30) and the association between the determinants in our study and the screening coverage was consistent with the literature. Therefore, the findings in this study can demonstrate the disproportional impact of SES on women who have different breast cancer screening rate and can inform the resource allocation in policymaking. Another potential limitation of this study was the exclusion of neighborhoods that have less than five screened women, which was mainly related to the small size of a neighborhood. This measure was taken by the breast cancer screening program administrators with the aim to protect privacy and is mandatory by the Flemish government. However, we think that the effect of this exclusion was limited due to the fact that we included 92% of all neighborhoods (31).

Women in neighborhoods that have a relatively low SES, that are characterized by being an immigrant with a foreign nationality, and having a large average household size, as well as women in neighborhoods that have a relatively high SES, that are characterized by a high average personal annual income, participate less frequently in the BCSP. On the other hand, women who belong to neighborhoods with a relatively high SES tend to participate more in the opportunistic screening. Tailored intervention that aims to increase the coverage of BCSP should pay more attention to women in these neighborhoods.

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author/s.

Ethical review and approval was not required for the study on human participants in accordance with the local legislation and institutional requirements. Written informed consent for participation was not required for this study in accordance with the national legislation and the institutional requirements.

LD, MJG, GB, and GV conceived the study, performed the data analysis, and wrote the manuscript. SJ was involved in the data curation and review of the manuscript. KV, MG, HD, and PM wrote the manuscript and verified the analysis. All authors discussed and interpreted the results and contributed to the final manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.