1. Introduction

The risk of developing breast cancer over a woman’s lifetime depends on characteristics such as age, breast density, family history of breast cancer, history of benign lesions, or genetic predisposition, among other factors. The difference in risk can be substantial between two women based on these characteristics. However, population-based breast cancer screening is based solely on age. It is in this context that it has been proposed to evaluate the effectiveness of screening based on a woman’s individual risk [1].

There is still no evidence to suggest that personalized breast cancer screening is no worse than or potentially better than current screening in reducing breast cancer mortality [2]. Specifically, there is insufficient evidence to demonstrate that the primary goal of screening, which is to detect the killing cancers early, can be improved for all women with a personalized model that screens higher risk women more frequently and lower risk less frequently. However, it is suggested that this strategy could increase the benefits and reduce the harms of current screening overall. Two prospective multicenter randomized controlled trials are being developed internationally to generate evidence on the effectiveness of personalized screening in reducing breast cancer-specific mortality compared to current screening (Wisdom in the US and MyPeBS in Europe and Israel) [2,3].

Stratified breast cancer screening estimates individual breast cancer risk by using various risk factors and proposes recommendations (screening interval, start age, and type of tests) to be tailored to different risk groups [4]. Several models are available for predicting and stratifying risk and generally include age, family history of breast cancer, previous benign breast conditions, breast density, and polygenic risk scores [5].

Both MyPEBS and WISDOM use three main levels for risk stratification: higher, average or medium, and lower risk, based on the probability of developing cancer in the next five years. In MyPeBS for the highest risk group, a mammogram (or MRI for dense breasts) every year is recommended for the higher risk group, a 2D mammogram (or tomosynthesis for dense breasts) every two years is recommended for the average risk group, and a 2D mammogram every four years for women at lower risk than the average. This group of women is particularly relevant as a longer screening interval can improve specificity but does not guarantee the same sensitivity. Overall, it is expected that sensitivity will be increased in the highest-risk group without significantly compromising specificity (false positives), and specificity will be increased in the lowest-risk group without significantly compromising sensitivity, particularly in the detection of early-stage breast cancers. Based on the values and expectations of women, healthcare professionals and other stakeholders, compromising the sensitivity of screening is of greater importance than compromising specificity.

In addition, personalisation increases complexity due to the socialisation of the message and its communication to women, which makes the role of healthcare professionals essential in explaining complex concepts such as relative and absolute risk reduction, overdiagnosis and false positive results. Furthermore, complexity increases for future implementation of personalized screening, as it will increase the workload of professionals, it will require additional staff training and poses challenges for extending the intervals between screening tests [3]. These challenges include one of the most complex issues in implementation: the potentially lesser acceptance of extending screening intervals among women estimated to be at lower risk [4,6]. In turn, this low acceptance seems to involve various factors, including women themselves (their beliefs, fears, knowledge, attitudes, experiential knowledge), the healthcare professionals and system’s organisation, and the personalised strategy itself [7]. All these considerations could hinder the transition to a new screening strategy, as personalisation must be acceptable to different stakeholders involved from the clinical, social, and ethical points of view [8].

Healthcare professionals play a determining role in the implementation of the new screening strategy, as their perceptions may influence women’s acceptability and decision to participate; therefore, getting closer to their opinions regarding this screening approach will contribute to the effective of the implementation [9–12].

There is limited evidence on the opinions of healthcare professionals involved in personalised screening projects regarding the acceptability of this strategy. In general, opinions are positive, considering it a logical step in breast screening. They believe that this strategy will particularly benefit high-risk women by increasing the frequency of screening, reducing mortality from the disease and increasing the survival of women diagnosed. For lower-risk women, they report a reduction in overdiagnosis and false positives. These advantages will increase the efficiency and effectiveness of the use of healthcare system resources. The main disadvantages highlighted are the potential resistance of lower-risk women to the recommendation to reduce the intensity of mammographic screening [13,14].

Only the BC-Predic project in the United Kingdom has thoroughly investigated the views of those involved on reducing screening intensity. Health care professionals consider this logical, but they are cautious in recommending it due to doubts about the accuracy and stability of risk estimates and the increase in interval cancers, as well as a misperception among women that lower risk is synonymous with no risk [15].

The aim of this study was to explore the views of healthcare professionals involved in the MyPeBS trial on the acceptability of a personalised strategy for breast cancer screening in women deemed at lower risk.

2. Materials and methods

3. Results

4. Discussion

We summarised healthcare professionals’ views on the acceptability of a personalised breast cancer screening strategy in lower-risk women. Our results are consistent with previous findings indicating a high acceptability of personalised breast cancer screening, which decreases with the recommendation to widen screening intervals [10,18]. However, it also offers novel and different perspectives on this issue to those already reported.

This study was conducted in the context of the MyPeBS study, which aims to improve the evidence on the effectiveness of a personalised screening strategy based on individual risk by increasing sensitivity in women at higher risk without compromising the diagnosis of early stage breast cancers in women at lower risk. The aim of this study was to analyse the opinion of healthcare professionals, assuming that this hypothesis is met, but with the uncertainty that it has not been confirmed.

In this sense, healthcare professionals in our study described “uncertainties” about the future implementation of a lower-risk pathway. Perhaps the most compelling doubt, and not unique to our study, is the need for stronger evidence of the benefits and safety of personalisation in lower-risk women compared with current screening [15], which is the main goal of MyPeBS trial [2].

This uncertainty makes them “wary” of recommending less frequent screening for fear of an increase in interval cancers, and consequently reduce sensitivity [15]. In this situation, Australian healthcare professionals have questioned whether the benefits of personalised screening would outweigh the harms, and whether its implementation could be justified without strong evidence and clear guidelines [19].

Participating healthcare professionals identified women’s previous participation in population-based and/or opportunistic screening as the most influential factor in this lesser acceptability, which has not previously been documented in studies exploring the acceptability of a lower-risk pathway. This, in turn, relates to another factor that emerged in the study: the safety that biennial mammography screening engenders for women.

This desire for “safety” has become one of the most documented factors in the resistance to the introduction of new screening strategies [6]; confronting women with a choice between the “safety” versus “advantages” of personalisation (possibility of individualised early detection and a better balance of benefits and harms) [15,20]. For this reason, several authors have proposed that women choose the screening modality as a way of offering them peace of mind [14] and to increase the acceptability of personalised screening [6].

In turn, the “safety” provided by biennial mammography is enhanced by another factor identified in our study that has not been previously documented: the message of “essential surveillance” through annual mammography screening that is indirectly disseminated by private healthcare through women who have access to these services. This message is problematic because it becomes part of the construction of women’s “experiential knowledge” about breast cancer and screening [21]. It contradicts the public health message, jeopardises women’s participation in screening and their relationship with their primary care physicians [22], thus hindering the effective implementation of personalised screening [18]. This also includes fear of breast cancer, which continues to shape responses to the disease and participation in screening. Two European studies suggest that despite a high level of knowledge about the disease fear levels are high, prompting them to undergo more frequent screening, or even seeking for early detection when population based screening is not offered in women younger than 50 years [23,24]. This fear has been amplified by the media, which emphasises the benefits of screening rather than its harms and leads to participation driven more by emotional than rational factors [25].

Other “uncertainties” about implementation highlighted by participants were the optimal way to communicate lower risk. They consider this key to women’s understanding and informed decision-making. This challenge has been reported in other studies, highlighting the complexity faced by health professionals when conveying lower risk. Often, lower risk is perceived as no risk, making breast cancer as an irrelevant concern [10,26]. Finally, they drew attention to the fact that risk communication requires more time than that allowed in typical consultation and the availability of qualified health professionals [11].

Our results are also consistent with other reported concerns, such as women’s willingness to provide personal and genetic information [13], ensuring equal participation of all women, poor training of professionals in personalised screening and elements of genetics [27,9], and the shortcomings of public health systems, which may have a negative impact on the feasibility of implementation in terms of human, financial, and structural resources [15,28].

If the findings from MyPeBS support wider screening intervals for lower-risk women, we need to promote acceptability among these women with the use of various tools and the adaptation of styles and formats to the levels of health literacy to provide information on personalisation and communicate risk [18,26]. Ensuring that women understand information on personalisation will key to ensuring equitable access for all women [6,8]. This is especially relevant in a multi-ethnic setting such as Catalonia, where large migratory processes contribute to the diversity of languages, cultures, religions and levels of health and digital literacy; these factors may affect women’s understanding of estimated risk and screening recommendations.

However, in addition to adequate risk information and communication, it is also necessary to develop strategies to provide follow-up and “support” to lower-risk women during the intervals between mammograms. Thus, face-to-face meetings with health professionals, reminder letters, helplines and websites are strategies proposed for this purpose and are consistent with the results of other studies [15].

Another essential and pressing issue raised in the study is the need to train primary care professionals, given the decisive role they will play in implementing a personalised screening model [29]. Two large studies reported that these professionals lack sufficient knowledge and need further training [30,31]. Dunlop et al [32] emphasised that training them to carry out a change in practice would be a challenge that involves taking into account their diverse activities and roles, and time constraints.

On the controversial issue of perceiving the decrease in screening frequency as a cost-cutting exercise by the public health system, it is essential to recognise and explicitly state that this is partly due to “reallocation of resources” for high-risk women, but that its primary motivation is safety and harm reduction in screening tests [14]. The above is closely linked to the necessary collaboration between the healthcare system, the media and patient organisations to create information and educational initiatives to facilitate the understanding of personalised screening and the extension of screening intervals in lower-risk women [33].

In order to inform, educate and socialise women about personalised screening strategies, community initiatives such as patient associations and the “expert patient” strategy could be beneficial, as they have proven to be valuable sources of information and support and promote a ‘sense of community’ among women [34,35]. Although little reported in the literature, these community-based initiatives are crucial to reduce disparities in breast cancer screening by addressing the challenges and barriers faced by underserved populations. By focusing on the local setting, these initiatives interact with their communities and tailor interventions to their needs, building trust and awareness, as well as increasing the uptake of screening services [36]. In addition, working with community leaders to tailor health messages would help promote the participation of women from ethnic minorities [26].

Emerging evidence supports the feasibility of risk-based breast cancer screening. The WISDOM Study has demonstrated that personalized screening can effectively stratify women according to their risk while remaining safe and acceptable to participants [3]. These findings provide essential support for the transition from age-based to risk-stratified screening strategies, although further refinement of risk prediction models and risk-reducing recommendations as well as effective risk communication to patients and health care professionals are still needed for large-scale implementation. Importantly, reducing the frequency of screening in women at lower risk needs to be monitored to avoid losing sensitivity in the detection of early stage breast cancers.

5. Conclusions

Although our results are largely consistent with other previously published studies, they offer novel and relevant insights into the factors influencing the acceptability of women deemed to be at lower risk of breast cancer and recommendations for increasing the acceptability of personalisation. Future research should further examine the recommendations made and assess their feasibility. In addition, studies are needed to investigate the views of primary care professionals and women on extending screening intervals, and to propose strategies to promote acceptability for women deemed to be at lower risk.

Supporting information

Acknowledgments

The authors acknowledge the healthcare professionals who participated in this study. They also acknowledge the MyPeBS Executive Committee, listed here in alphabetical order: Jean-Benoît Burrion, Suzette Delaloge, Sandrine De Montgolfier, Fiona Gilbert, Livia Giordano, Paolo Giorgi-Rossi, Michal Guindy, Harry De Koning, Cecile Vissac-Sabatier.