STRENGTHS AND LIMITATIONS OF THIS STUDY

The study provides multiple perspectives on barriers to cervical cancer screening towards women in vulnerable situations from stakeholders from seven European countries with different proficiency of cervical cancer prevention.

Involving multilevel stakeholders ensured relevant findings for vulnerable women’s needs and healthcare systems, enhancing research applicability to real issues.

The study has a robust sample size (n=120).

A limitation was differences in numbers of representation of micro-level, meso-level and macro-level participants in the respective countries.

Introduction

Cervical cancer (CC) causes approximately 300 000 deaths per year worldwide1 and in 2020, there were 58 169 new cases and 25 989 deaths caused by CC in Europe alone.2 Regular screening is key to reducing mortality from CC.3 However, screening and human papillomavirus vaccination coverage is significantly lower in women from vulnerable and underserved groups than those from higher income groups, placing the former at a greater risk for CC.4 Only a few and primarily Northern and Western European countries have designated policies to broaden coverage among vulnerable groups.5 Thus, it becomes crucial to understand the local barriers that prevent the uptake of a preventive service by those who need it the most.

A recent scoping review about perspectives on barriers to cervical cancer screening (CCS) towards vulnerable women showed that barriers include (1) financial barriers and mistrust in the system, (2) lack of information about CC and CCS pathways and follow-up and (3) lack of awareness about CC and CCS, fear, and lack of attention to preventive care in general. The studies concerning barriers covered by the review were undertaken in 11 different countries. 22 of the studies came from stakeholder perspectives on different decisional levels.6 The importance of including the perspectives of the most underserved populations in research has long been recognised.7 The scoping review showed that most of the studies elicit women’s perspectives from ethnic minority or migrant groups (n=20).8–28 Perspectives from women in other vulnerable situations included women living with substance abuse (n=1)29 and women who had experienced sexual abuse.30 Three of the studies included perspectives from providers and women in vulnerable situations18–20 and two studies provided the perspectives of providers only.31 32 In summary, the perspectives of several subgroups of vulnerable women remain underexplored, as do the perspectives of healthcare providers, social workers and decision-makers.

According to Braveman and Gruskin,33 inequity systematically disadvantages people who are already disadvantaged in terms of their health.

The present study is nested in the European Union-funded project CBIG-SCREEN which aims to tackle inequity in CCS for vulnerable women and create a European-wide knowledge framework around barriers to CCS (www.cbig-screen.eu).

The aim of this study was to elicit the perspectives of all levels of stakeholders in a cross-cultural comparison of barriers in seven European sites.

MethodsSetting

The study took place in Bulgaria, Denmark, Estonia, France, Italy, Portugal and Romania. These countries differ in socioeconomic status (SES), CC epidemiology and prevention approaches (table 1).

Table 1

Overview of setting per country

Design and recruitment

We used a qualitative, participatory approach by establishing Collaborative User Boards (CUBs) in the seven European countries. We designed CUBs to establish a safe space for mutual learning and exchanging views and experiences between stakeholders across professional and social boundaries. Furthermore, the purpose of the CUBs was to inform the development of tailored interventions for women in vulnerable situations to tackle inequity in CCS as a part of the CBIG-SCREEN project. We draw on the tradition of patient and public involvement in terms of involving stakeholders in healthcare research.7 The participants were involved at the level of consultancy.34

The CUBs were designed to comprise stakeholders with vested interest in CCS directly or indirectly affected by a problem and/or having the power to influence solutions. Three levels of stakeholders should be represented in a CUB: micro level (the users and representatives of the target groups affected by the problem), meso level (representatives of professionals who work with the target group or with screening programmes) and macro level (policymakers and decision-makers who have the authority to influence the problem). The voices of the stakeholders should be equally weighed.

In the recruitment process, vulnerability was understood from an etic perspective based on epidemiological principles of identifying groups at risk. However, with the inclusion of representatives of vulnerable groups, the intention was to gain an emic perspective on vulnerability, which includes personal perceptions of challenges in CCS.35

The local research teams in each country defined eligible participants for the CUBs using both purposive and snowball sampling.36 Decisions on the eligibility of vulnerable groups were guided by a survey undertaken within the CBIG-SCREEN project where experts and programme managers defined their countries’ most vulnerable and underserved subgroups.5 To adapt to the local context, it varied from country to country whether the participants were reimbursed for their participation.

Data collection and analysis

To align the content and structure of the CUB meetings, local researchers from each country participated in a 2-day workshop in Denmark in September 2021 where a standard guideline for the conduction of CUBs was introduced and hereafter adapted to the local contexts. The local research teams developed a range of ways to prompt discussions in CUBs in collaboration with the other teams through discussions at online meetings between October 2021 and June 2022. The prompts included presenting barriers identified in scientific literature, infographics about CCS pathways, video-recorded or audio-recorded interviews with vulnerable women, group work and icebreakers.37

Between February and June 2022, the CUB meetings took place in each country using the local language. Each meeting lasted approximately 2 hours. We used focus group techniques either with the use of predefined topics or interview guides, where participants were encouraged to discuss their perspectives on barriers in CCS for vulnerable women or solutions and enablers. Results concerning solutions and enablers will be reported elsewhere. To provide flexibility and adaption to local context, each research team decided whether the CUB meeting would be delivered as a face to face, online or hybrid. The project was initiated in the aftermath of COVID-19, and in Italy, for instance, people were still reluctant to meet face to face. In table 2, we provide an overview of the number of meetings and how they were organised in each country.

Table 2

Overview of the organisation of CUBs

We were cautious about providing a safe space for discussions and ensuring that the CUB meetings accommodated all participants’ needs. We were aware of potential asymmetric power relations between researchers and participants as well as between the participants. Considering that micro-level participants were individuals with current or former vulnerable life situations, we were particularly precautious about making them feel comfortable at the CUB meetings by providing them with tailored information about the project, making sure that there was a familiar healthcare professional or social worker present and by preparing them for their role as informants at premeetings. We took these precautions to ensure that they felt safe expressing themselves without repercussions.

The local research teams transcribed and translated audio recordings and video recordings of the CUB meetings, then sent them to the first author using an encrypted connection who finally imported to the qualitative data management software NVivo to manage and analyse the data.38 Data from the meetings focusing on solutions were included in the dataset because barriers were also discussed during these meetings. The analysis was inspired by the framework analysis method by Ritchie and Spencer.39 This approach is useful for analysing and comparing large and complex qualitative datasets deriving from different jurisdictions and geographical contexts.40 Initially, the first author was familiarised with the data organised by country. This included initial coding and adding commentaries of ideas of concepts and themes to the data. Next, developing the framework for analysis took place in an iterative process. The first author coded the dataset from three countries inductively focusing on discussions about barriers directly related to CCS or affecting vulnerable women’s participation in CCS in a continuous discussion with the last author. Then, the framework was deductively applied to the remaining data. The framework continued to develop throughout the analysis. When the coding was finalised, we summarised the data into abstracted themes and subthemes then charted for comparison. Finally, the codes were mapped into clusters based on similarities in the participants’ perceptions of barriers between countries and then interpreted.40 For validation and understanding of context, the interpretation of data was discussed with co-authors from all participating countries.

Patient and public involvement

The voices and perspectives of stakeholders directly impacted by the lack of optimal CCS for vulnerable women were emphasised in this study. The perspectives have the potential to be incorporated into decision-making and the development of interventions to influence future healthcare services and policies. During the CUB meetings, the participants were actively encouraged to share their thoughts, concerns and experiences related to barriers towards CCS. In this way, involvement played a central role in ensuring that the perspectives of those directly impacted were captured.

Results

We included a total of 120 participants, including 39 micro-level, 63 meso-level and 18 macro-level stakeholders (table 3).

Table 3

Level of representation and distribution of participants across the seven countries

We identified individual-level, provider-level and system-level barriers (table 4).

Table 4

Barriers elicited by the stakeholders in each country

At the individual level, barriers included emotions like shame and fear, stigma, lack of knowledge about CCS, difficulties with understanding healthcare information and the concept of CCS, practical challenges such as logistics and lack of time or childcare, and financial issues like travel expenses and lack of health insurance. Barriers at the provider level included insufficient involvement of medical doctors in CCS, lack of cultural and relational competencies in dealing with vulnerable populations, lack of resources and training and unclear communication about test results and implications. System-level barriers included the lack of a national, organised screening programme, inadequate registries, problems with monitoring due to opportunistic and private screening offers, the lack of individualised care and a low priority given to preventive healthcare.

We identified similarities and differences in perceptions of barriers in clusters of countries (see the online supplemental figure). In all countries (cluster 1), participants appointed vulnerable women’s feelings of shame and lacking priority of prevention due to their life situation. We found differences in participants’ perceptions of barriers between clusters 2 and 3. Perspectives from participants in Denmark, Estonia, France, Italy and Portugal constituted cluster 2. They shared similar perceptions of barriers including difficulties accessing women, providers’ insufficient cultural and relational competencies and vulnerable women’s insufficient health literacy. Perspectives from participants in Bulgaria and Romania constituted cluster 3. The perceived barriers included lack or insufficient organisation of CCS, lack of population registry linked with screening registry, lack of medical doctors in remote areas and financial barriers.

Excerpt examples underpinning the results are presented in table 5 and referred to by number.

Table 5

Examples of underpinning excerpts

Cluster 1: perspectives from participants in all countries

In all countries, barriers at the level of the individual included feelings of shame deriving from cultural and religious beliefs and norms. This included shame related to privacy and exposure of intimate body parts to male providers (France, Bulgaria, Denmark, Italy and Romania) (excerpt 1), shame related to the association between CCS and sexual activity (Estonia) and shame related to ethnicity (Portugal) (excerpt 2).

In Denmark, Estonia, Italy, France and Portugal, shame was associated with the women’s life situation and fear of stigma and of exposing their life situation because of bad hygiene to both healthcare staff and other patients in the doctors’ waiting room (excerpts 3, 4, 5).

Furthermore, the participants emphasised that women living in difficult situations have other priorities than health and prevention. They live their lives from day to day and substance abuse or basic survival is of the highest priority (excerpts 6, 7, 8)

In Romania and Bulgaria, the participants pointed out that in certain subgroups, there is a culture of ignoring symptoms and not attending healthcare services (excerpt 9). In Italy, the participants emphasised varying cultural beliefs about preventive healthcare. In Denmark, there was a belief that effective treatment in the healthcare system makes preventive healthcare including CCS superfluous (excerpt 10). In Romania, Bulgaria and Portugal, the participants identified neglect and disinterest in CCS as the main barrier (excerpt 11).

Cluster 2: perspectives from participants in Denmark, Estonia, France, Italy and Portugal

Participants in cluster 2 countries identified incorrect or missing information about email and postal addresses in population registries as a primary barrier (excerpt 12). Moreover, they emphasised that healthcare providers’ attitudes towards vulnerable populations were rooted in a paternalistic approach to the clinical encounter leading to condescending behaviour. Previous encounters with insensitive providers possibly prevented women from attending CCS (excerpts 13, 14).

Vulnerable women’s lack of knowledge and health literacy was perceived as barriers from the perspective of both vulnerable women and providers. Women experienced that they lacked knowledge of CC and CCS and that information was not provided (excerpt 15). This included lacking knowledge of eligibility criteria with women considering themselves eligible due to sexual inactivity, only having one partner, considered themselves too old, having no symptoms or because they had no family history of cancer (excerpt 16). Providers experienced that vulnerable women lack the health literacy to understand the information provided by health professionals and authorities (excerpt 17). This was related to women’s varying levels of education and basic knowledge of the human body (excerpt 18).

Cluster 3: perspectives from participants in Bulgaria and Romania

In cluster 3 countries, participants’ perceptions were that the organisation of CCS was the main barrier for all eligible women not only those in vulnerable groups.

In Bulgaria, only opportunistic screening was offered and primarily to well-educated women. The participants reported that some medical doctors advised women to be screened more frequently than recommended by guidelines because of financial advantages (excerpt 19). In Romania, the participants pointed out that the whole screening pathway was inadequate owing to the lack of screening registry, which impedes the possibility of inviting and providing the women with test results (excerpt 20).

Participants in both countries emphasised that shortage of medical doctors involved in CCS as a barrier.

In Romania, only a few general practitioners (GP) were involved in mobilising vulnerable women to attend CCS. Barriers to GPs’ active involvement included lack of time financial incentives (excerpt 21).

In Bulgaria, the barriers include a shortage of doctors in remote areas, GPs not tasked with CCS or funded by health insurance and low priority of preventive healthcare in the population and among policymakers (excerpt 22). Furthermore, a general mistrust of medical doctors due to corruption and increasing commercialisation was identified as a barrier. Participants similarly pointed to lack of funding or partly funded PAP smear as a barrier. In Bulgaria, mainly women with health insurance were served in opportunistic screening even though participants implied that testing should be free of charge for all (excerpt 23).

In Romania, low SES and a lack of health insurance were considered barriers to equal access to follow-up treatment. Women with higher SES could enter the private system or to do follow-up in the public health services, whereas women with lower SES were left without possibilities for treatment. In Romania, participants emphasised that funding of CCS partly through national public funding and partly through European funding programmes created significant differences within the country depending on the involvement of local health authorities and the time span of the shorter funding programmes.

Discussion

This study identified stakeholder perspectives on barriers towards CCS for vulnerable women and mapped them according to similarities in clusters of countries. The findings suggest that vulnerable women share similar barriers regardless of the healthcare system or their life situations.

In all countries, participants emphasised that vulnerable women tend to place preventive healthcare low on their list of priorities due to the difficulties they face in their everyday life and low health literacy. This is supported by an American study which found that high-risk and low-income groups have a much lower engagement in standard preventive healthcare services than other groups.41 The systematic review conducted within the CBIG-SCREEN project6 identified several reasons for vulnerable women’s low priority of preventive healthcare including childcare, work, pressure following substance abuse, complex migration processes and low self-esteem.

We found that women from all countries experienced feelings of shame related to exposure of their bodies during testing however differing in reasons depending on culture and the type of vulnerable situation they face. Feelings of shame connected to CCS are a well-known barrier for women regardless of nationality and SES. The linked systematic review6 found that embarrassment and fear of stigma were perceived as barriers to attendance in CCS for subgroups of vulnerable women in 18 of 33 articles. In a UK population-based survey, Waller et al 42 found that, in general, embarrassment was the most common barrier to attendance.

The findings in our study indicate that stakeholders in countries with lower gross domestic product (GDP) experience barriers that are important for the provision of CCS for all eligible women including vulnerable women. Perceived barriers in countries with higher GDP are related to encounters with vulnerable women and their specific needs. We found that Bulgaria and Romania, which have the lowest GDP, mainly share barriers that are important for the provision of CCS and include lack of functioning population registries or linkage with screening registries impeding targeted invitations to women, shortage of staff and financial barriers among women associated with low SES and lack of healthcare insurance. The latter was similarly identified as a barrier within breast cancer screening in vulnerable populations.43 In Denmark, Estonia, France, Italy and Portugal, which have higher GDP, the common barriers are related to providers’ insufficient cultural and relational competencies in encounters with vulnerable women. According to McCormack et al,44 the need to integrate person-centred approach in healthcare has long been recognised. However, integrating a person-centred care for all people requires a cultural paradigm shift. McCormack et al 44 argue that person-centred healthcare is difficult when healthcare organisation is based on individual responsibility and complex models of insurance-based services. This ties well with our findings concerning financial barriers in Bulgaria and Romania where discussions about individualised care were absent and where partly funding and the dependence on health insurance were seen as substantial barriers towards CCS for vulnerable women, particularly women with low SES.

Interventions to address and overcome perceived barriers in CCS must be tailored to vulnerable women’s specific needs. However, the similarities in stakeholders’ perceptions of barriers between countries found in this study provide a picture of tendencies at a European level for decision-makers to consider. The inclusion of the voices of both vulnerable women and other stakeholders with a vested interest in promoting CCS for vulnerable women could pave the way for more feasible interventions.

Strengths and limitations

A main strength to this study was the inclusion of multiple voices across countries and professional and social boundaries providing stakeholder perspectives on both individual, provider and system levels.

Another strength is that the study brings novelty to the field of knowledge by providing a comparative Pan-European overview of barriers based on stakeholders’ perspectives with a robust sample size (n=120).

Each local research team developed and adapted the CUB format co-creatively with the other local research teams in other countries. The synergy from this co-creative process was a strength and translated into how the CUBs were locally organised and conducted.

Comparing stakeholder perspectives in countries with different cultures, demographics, social security systems, healthcare systems and maturity of CCS may seem like a limitation. Nevertheless, the comparison has provided an overview of perceived barriers and revealed similarities across countries, particularly at the level of vulnerable women regardless of their country of residence.

A limitation of the study was the differences in representation in the respective countries. The local research team in each country defined the participants for the three levels of representation. In particular, the macro-level representatives varied in the types of their positions depending on power distribution in the respective countries. For instance, France, where decisions on CCS and vulnerable populations are made at a ministerial level,45 ended up without macro-level representatives, because invitations to the ministry and other national health regulatory agencies were rejected. Denmark represents a country where decisions are decentralised to regions and municipalities46 and included macro-level representatives holding positions as heads of hospital departments and local politicians.

The first author primarily conducted the analysis on data from all countries but was neither present during data construction nor natively familiar with national contexts or cultures besides her own. This possibly affected the interpretation of data. However, the interpretations were validated by local research members in each country.

Conclusion

The foundation for developing targeted CCS programmes for subgroups of women in vulnerable situations is to understand the mechanisms preventing women from attending. With continuous inequity in CCS, there is a need to integrate stakeholder perspectives in developing interventions to improve services along the CCS pathway. This study provides an overview of similarities in perceived barriers across countries, professions and social boundaries in seven European countries.

At an individual level, vulnerable women share similar feelings of shame and a lack of focus on prevention in healthcare regardless of their vulnerability. Perceptions of barriers at the provider and system levels are related to GDP, the organisation or lack of screening programmes, demographics and the general approach to vulnerable people in healthcare. In countries with a higher GDP, perceived barriers are related to healthcare providers’ approach to vulnerable populations. Both findings point in the direction of improving healthcare providers’ cultural sensitivity and communication skills. In countries with lower GDP, the perceived barriers are more likely to be related to the lack of or inadequate healthcare funding and provision of CCS which requires fundamental system-level changes in the delivery and financing of healthcare.

This study will inform future interventions within CBIG-SCREEN to improve CCS for vulnerable women and reduce inequity. Stakeholders’ suggestions of solutions to barriers in CCS will be reported in another article.

Data availability statement

Data are available upon reasonable request.

Ethics statementsPatient consent for publication

Not applicable.

Ethics approval

Ethical approval was obtained by local committees when required: Bulgaria (the Bulgarian Sociology Association), Estonia (Research Ethics Committee of the University of Tartu; 359T-22) and Portugal (Instituto de Saúde Pública da Universidade do Porto ethics committee; CE22206). Written informed consent was obtained from participants in all countries including consent for publication except from Romania where only the representatives of vulnerable women signed an informed consent in accordance with Babes-Bolyai University Ethical Committee regulations.