What factors influence the uptake of bowel, breast and cervical cancer screening? An overview of international research

Abstract Background For cancer screening programmes to be effective in early detection it is important that those invited can access screening services and understand the benefits of participation. A better understanding of the factors that matter to potential participants of cancer screening programmes can assist in developing strategies to increase current uptake. Methods We conducted an overview of systematic reviews to answer the question: What factors influence the uptake of cancer screening services (breast, bowel and cervical) in high-income countries? A thematic approach supported by tabular summaries and qualitative heat maps was used to categorize factors, described as ‘barriers’ or ‘facilitators’. Results A total of 41 systematic reviews met the criteria for inclusion. The barrier with the greatest number of ‘hot spots’ across all three screening programmes was a fear of the unknown regarding a possible diagnosis of cancer or abnormal screening results, followed closely by a general lack of knowledge surrounding cancer screening programmes. The greatest collective facilitator to uptake was recommendation by a healthcare provider to attend screening. Conclusion Across all factors ‘trust’ and ‘building trusted relationships’ can be seen as integral to the success of cancer screening programmes and must be reflective of collaborative efforts to mitigate barriers and enhance facilitators to uptake. There is future scope to consider interventions that (i) increase demand for screening services, (ii) reduce barriers to uptake of services and/or (iii) are relevant to the healthcare system and those providing services.


T
he National Health Service (NHS) in the UK provides population-based screening programmes for bowel, breast and cervical cancer which are free to access and aim to detect cancer or precancerous activity in asymptomatic individuals.For screening programmes to be effective in early detection it is important that those invited can access screening services and understand the benefits of participation.
2][3] Screening uptake has been shown to correlate with the number of cancers diagnosed at an earlier, and more treatable, stage. 4,5Invitations from the NHS are currently issued by age and at periodic intervals: 6 i.Breast screening is offered to anyone registered with a general practitioner as female between the ages of 50 and 70, every 3 years.ii.In England, everyone aged 60-74 is offered a bowel cancer screening home test kit every 2 years; in Scotland, the age range is 50-74 years and 55-74 years in Wales.iii.Cervical screening is offered to all women and people with a cervix every 3 years for those aged 25-49, and every 5 years from the ages of 50-64.
Early diagnosis through screening improves health outcomes for patients and lessens the burden of required resources within a healthcare system. 7A better understanding of the factors that matter to potential participants of cancer screening programmes can assist in developing strategies to increase uptake.This overview of systematic reviews aims to address the question: What factors influence the uptake of cancer screening services (breast, bowel and cervical) in high-income countries?Studying factors within all three cancer screening services offers the opportunity to reflect on programmes individually and identify commonalities.

Methods
We conducted an overview of systematic reviews and registered the research protocol into PROSPERO, the National Institute for Health and Care Research International prospective register of systematic reviews (registration identification: CRD42023403479).The overview was guided by the recommendations of the Cochrane Handbook for Systematic Reviews of Interventions and the Joanna Briggs Institute (JBI) Manual for Systematic Reviews.We used the JBI Checklist for Systematic Reviews and Research Syntheses to account for the inclusion of qualitative and mixed-methods systematic reviews. 8

Search strategy
A comprehensive search strategy was developed with the assistance of an information specialist and is presented in Supplementary material 1. MEDLINE (Ovid), the Cochrane Database of Systematic Reviews, and the Database of Abstracts of Reviews of Effects were searched for systematic reviews and systematic scoping reviews published from 01 January 2012 to 31 January 2023.A 10-year period was selected with our NHS partners to best capture the most relevant factors related to uptake in the context of modern screening programmes.No language restrictions were initially applied, with English language used as the final limiting filter.Searches were not rerun prior to the final analysis.

Eligibility criteria
This overview is international in scope and focussed on high-income countries with healthcare systems similar to the UK.The World Economic Situation and Prospects 2023 report from the United Nations was used to identify countries classified as high-income. 9eviews for inclusion focussed on factors that matter to potential participants of bowel, breast and/or cervical cancer screening programmes.It was agreed that screening must be the primary focus, not a wider component, of included reviews.
Reviews were excluded if studies were not exclusively conducted in high-income countries, incorporated indications other than bowel, breast and/or cervical cancer, focussed on genetic cancer screening (e.g.BRCA1/BRCA2, Lynch syndrome), or highlighted screening procedures beyond routine uptake.Guidelines, economic analyses, and reviews of solely interventional research were not eligible for inclusion.

Data extraction
All citations retrieved through the search process were initially assessed by title and abstract based on the inclusion and exclusion criteria.One reviewer assessed all citations with each second reviewer blind assessing a differing 10% of citations, giving a total of 20%, to ensure consistency in the selection process.
All citations judged to be potentially relevant were retrieved in full and reviewed by one reviewer, with each second reviewer blind assessing a differing 10%, for a total of 20%, to ensure uniformity in the interpretation of eligibility criteria.Any disagreements or uncertainty during the selection process was resolved by consensus between reviewers.Citations and inclusion/exclusion rationale were recorded using Microsoft Excel.
A data extraction form was designed to capture review specifics such as search strategies and methods, details of included studies, and key findings including implications for future research.The full data extraction forms are available in Supplementary material 2.

Critical appraisal
The JBI Checklist for Systematic Reviews and Research Syntheses was used to critically appraise the methodological quality of included systematic reviews. 10It was agreed that Question 8 of the JBI checklist be amended to reflect the range of methods more broadly within the reviews and was modified to read: 'Were the methods used to combine and/or summarise studies appropriate?'.
Reviews were not excluded based on their methodological quality, which was assessed to inform the robustness of findings as well as identify common areas for methodological improvement across reviews.The results of the critical appraisal are included in Supplementary material 3.

Synthesis and analysis
We decided a priori to acknowledge the heterogeneous nature of the existing reviews, and to be guided by the evidence presented by the authors of the identified reviews when considering the diverse factors influencing the uptake of bowel, breast and/or cervical cancer screening.
Factors, commonly described in the literature as either 'barriers' or 'facilitators', were first identified and highlighted by one reviewer using NVivo 12.0 and then discussed collaboratively.As the presentation of results varied widely across reviews, only those factors that were described by the authors as integral or key to understanding were captured for further discussion.Factors were discussed in depth by the review group (SP, MB, ST) and organized in common categories as supported by previous similar research for vaccine uptake. 11ecoding of items that covered comparable content was performed by consensus.For example, 'physician recommendation as a cue to action', 12 'having a clinician recommendation for the test' 13 and 'healthcare provider recommendation' 14 were recoded to the wider line item of 'healthcare provider recommendation to attend screening'.It was agreed that monetary factors such as insurance or privatized healthcare, as noted in studies from the USA, would not be included in the analysis as these factors are not relevant within the context of NHS population-based screening programmes in the UK and other similar international counterparts.
All data were synthesized using a thematic approach as described above.A thematic approach was used to support an inductive process of coding by identifying, describing and interpreting themes within a multifaceted research question.Codes and descriptive themes were developed from the data to provide insights into factors influencing screening uptake.The thematic analysis is supported by tabular summaries and visual heat maps with factors frequently mentioned coloured red, and those rarely mentioned coloured green.Factors that were not mentioned are coloured grey.A red square is, therefore, a 'hot spot' for action (see Supplementary material 6).
Analysis of the implications and recommendations for future research as described by the authors of the reviews was also undertaken using the same methodology, with key ideas highlighted in NVivo 12.0 by one reviewer and further synthesized using a thematic approach with tabular summaries and supporting quotes.As this is an overview of systematic reviews in varying contexts, no metaanalytical synthesis of findings was undertaken.

Results
Figure 1 summarizes the results of the searches and selection process in a PRISMA-style diagram.We identified 1450 citations after the removal of duplicates.After title and abstract screening, 64 records were reviewed in full text with 41 systematic reviews included in the final overview.Of these, 16 reviews (39%) focussed solely on factors related to bowel screening; 15 (37%) on cervical cancer screening and 6 (15%) on breast cancer screening.The remaining reviews provided a combined synthesis of factors relevant to screening uptake in breast and cervical programmes (2/41, 5%) and bowel, breast and cervical programmes (2/41, 5%).

Description of the included reviews
The main characteristics of the included systematic reviews, which varied widely given the heterogeneous nature of the overview, are presented in Supplementary material 4. Sixteen reviews (39%) focussed on the uptake of screening as directly relevant to ethnicity, while an additional 10 reviews (24%) addressed under-served groups more widely.Geographically, 21 reviews (51%) incorporated studies from multiple high-income countries.Studies from the United States were included in most reviews (32/41, 78%) followed by European countries broadly (21/41, 51%).

Overview of factors influencing the uptake of cancer screening services in high-income countries
A total of 12 categories were used to delineate the factors influencing the uptake of cancer screening services.Within this categorization a total of 45 barriers were identified across all three screening programmes (see table 1) with 15 barriers (33%) common to all screening programmes.The barrier with the greatest number of 'hot spots' for low uptake across all three screening programmes was a fear of the unknown regarding a possible diagnosis of cancer or abnormal screening results.
The most reported barrier to the uptake of bowel cancer screening was an inadequate knowledge of the screening programme itself.Scheduling issues were the most common barriers for breast cancer screening programmes including forgetting to book or attend appointments, unsuitable appointment times, and time constraints such as work commitments or childcare concerns.Fear of the Factors influencing the uptake of cancer screening programmes unknown was the most observed barrier for uptake of cervical cancer screening programmes.
Fewer facilitators to the uptake of cancer screening were found within the reviews as shown in table 2. Twenty-nine facilitators were identified across 9 categories.Of these, 15 were common across all three programmes (52%) with the greatest collective facilitator to uptake being the recommendation by a healthcare provider to attend screening.
Support provided by family members and/or social networks along with a healthcare provider recommendation to attend screening were the most cited facilitators within bowel screening programmes.Acculturation, described by the reviews as the process through which a person or group from one culture comes to adopt the practices and values of another culture, was found to be the main facilitator of breast cancer screening uptake. 15This is reflective of the included qualitative data, as most of the reviews incorporating breast cancer screening (8/10, 80%) focussed specifically on the perspectives of one or more ethnic groups.The recommendation of a healthcare provider to attend screening was the greatest individual facilitator of cervical cancer screening uptake, with other key facilitators being practitioners who reflect the lived experiences of participants and options for procedural self-testing.

Key recommendations from the systematic reviews
Recommendations for future research and best practice were also collated and synthesized from the included systematic reviews.Five priority areas were identified as outlined in table 3.This includes maximizing the trusted role of healthcare providers, prioritizing patient-centred care and patient autonomy, culturally tailored health promotion, systematically reducing health inequalities through policy, and informed research design.Further illustrative summaries and quotes are available in Supplementary material 5.

Discussion
This overview of existing reviews aimed to capture the factors, defined as barriers and facilitators, to uptake within bowel, breast and/or cervical cancer screening programmes in high-income countries.However, there are clear practical differences in how the programmes are delivered that influence these factors.Bowel screening programmes reflected the most variability in process, offering screening options within a healthcare setting and self-testing options performed at home.Both physical and psychological discomfort were expressed as key barriers to uptake due to the invasive nature of some bowel procedures such as a colonoscopy or sigmoidoscopy.These options also require an element of preprocedure bowel preparation via laxative treatment and/or dietary changes.Test preparation difficulties were a noted barrier to uptake with one review suggesting the preparation element potentially impedes individuals from repeat screening. 23hile there was evidence for self-testing options as facilitators to bowel cancer screening, concerns raised by potential participants as barriers included completing the test incorrectly and the validity of self-test results. 24,25Some participants were found to prefer a colonoscopy as 'they believed it to be a more thorough examination'. 25These factors offer some insight when reflecting on the general lack of knowledge surrounding bowel cancer screening and subsequent facilitators to alleviate misunderstandings.For example, the use of pictorial communication in self-testing procedures was noted as a facilitator to address concerns when completing an immunochemical faecal occult blood test or faecal occult blood test. 24Both tests, which are widely integrated to screening programmes across high-income countries, involve a self-sampling of stool which is then typically returned to a lab for further diagnostic

Gradient colour key a
Least !Most observed a: Barriers that were frequently mentioned are coloured red, while those rarely mentioned are coloured green.Barriers that were not mentioned at all are coloured grey.A red square therefore, a hot spot for action.b: BO, Bowel; BR, Breast; CE, Cervical.
Factors influencing the uptake of cancer screening programmes review. 24,25Clear communication for self-testing procedures may also contribute to enhanced trust within the healthcare system, including alleviating fears of screening procedures and potential health outcomes.
There are no readily available global self-testing options for breast cancer screening.While self-administered breast exams are recommended by the NHS and other similar healthcare systems, ultimately a diagnosis cannot be obtained without further clinical investigations. 26][29][30] Scheduling issues were the most cited barrier to uptake, including perceived time constraints to attending a screening appointment and childcare concerns.These were closely followed by the barrier of distance to testing facilities.Two reviews that focussed on rural geographies identified lack of transportation as a key aspect when considering the distance to testing facilities. 28,31While interventions were not within the scope of the current overview, only one review discussed the use of mobile mammography to assist with resource concerns in relation to breast cancer screening. 28he barrier of fear was most clearly seen as related to cervical cancer screening.This referred to not only the potential of a cancer diagnosis but general fear surrounding the results of human papillomavirus (HPV) testing.Confusion also persists surrounding HPV screening vs. a Papanicolaou (Pap) test. 18HPV screening aims to identify the virus which may cause cell changes to the cervix and eventually lead to cancerous outcomes.In contrast, a Pap test looks for precancerous cell changes on the cervix itself that may become cancerous if not treated promptly.A positive outcome in both testing scenarios is not necessarily indicative of a cancer diagnosis, with differing treatment options available.Reviews were explicit in the need for better informed choice in cervical cancer screening to alleviate fears surrounding testing procedures and potential outcomes. 17,18,32he option for HPV self-sampling was also a potential facilitator of cervical cancer screening uptake.While self-testing options exist in some high-income countries, these are not yet readily available worldwide.Findings from a 2022 article focussed on the global use of HPV self-sampling for cervical cancer screening noted six highincome countries with self-testing approaches in national programmes and/or guidelines (Australia, Denmark, Finland, France, the Netherlands and Sweden). 33Multiple other countries, including those grouped as low-and lower middle-income, had also implemented self-testing approaches or were piloting new programmes. 33cheduling issues were a barrier for those attending cervical cancer screening which could be circumvented with the introduction of self-sampling options in the first instance.This approach has also been shown to better reach those with irregular access to health care or in areas where health facilities may be less accessible. 17,18istrust in the individual healthcare provider performing the test was observed in a broad capacity across all three programmes, most Gradient colour key a Least !Most observed a: Facilitators that were frequently mentioned are coloured red, while those rarely mentioned are coloured green.Facilitators that were not mentioned at all are coloured grey.A red square is, therefore, a hot spot for action.b: BO, Bowel; BR, Breast; CE, Cervical.
Table 3 Priority areas for future research and best practices in cancer screening programmes as identified by the reviews i. Maximizing the trusted role of healthcare providers

Recommendation
As illustrated in the reviews a. Health providers may require additional support and training to enhance their knowledge of cancer and screening programmes.Effective training includes awareness of barriers to screening within underserved groups, consistently identifying those at higher risk of cancer such as first-degree relatives, and up-to-date knowledge on relevant screening guidelines and policies.
' … there is an urgent need for basic education surrounding the healthcare needs of gender minority patients [assigned female at birth], so that clinicians are responsive to each individual's needs and skilled in a range of approaches to cervical cancer screening.' 42Communication skills have been identified by the reviews as integral to improving overall willingness to attend screening and satisfaction with screening services.Healthcare providers should be made better aware of the impacts both at the personal and public health levels of their endorsement to attend screening.
'The patients' decision to attend screening is directly influenced by their encounters with healthcare staff.There is, therefore, a real need to better educate healthcare staff on the public health implications following their patient interaction'. 16Internal reminder systems for a primary care team may also be useful in ensuring recommendation for screening is delivered at appropriate intervals.
'The presence of an effective reminder system for the primary care team and for patients can also be helpful'. 43.Prioritizing patient-centred care and patient autonomy

Recommendation
As illustrated in the reviews a.The preferences of potential participants should be considered when undertaking cancer screening, including timely response to individual needs and values.Overarching patient-centred care strategies to increase uptake include considering the role of provider gender, language barriers, and differing lived experiences that may impact willingness to undertake cancer screening.
'Failing to account for the specific preferences of medically underserved individuals will allow the disparities in cervical cancer incidence and mortality to continue widening'. 17Individualized options for procedural processes may alleviate both physical and psychological distress associated with cancer screening.
' … increased emphasis needs to be placed on efforts to improve the bowel preparation process, enhancing comfort and modesty during the examination and identifying patients with significant anxiety beforehand'. 13c.Further educational materials, including complex terminology and/or visual aids, are needed to better inform the process of consent in cancer screening.
' … it is important for genuinely informed consent that people are not overwhelmed with information.Some terminology, for example, "high-risk HPV" and "wart virus", was confusing or alarming and not clearly understood.Explanations about causation, risk of cervical abnormality or cancer, persistence/clearance of monogenic HPV and difference from genital wart viruses are needed'. 18i.Culturally tailored health promotion

Recommendation
As illustrated in the reviews a.There is a lack of culturally tailored health promotion as a 'one-size-fitsall' approach fails to consider the heterogeneity within differing ethnic communities.Engagement strategies should be designed by and for specific communities, focussed on building trust and clear communication with available health services.
'Relevant programs should be aware of the importance of alternative sources in reaching the population as well as the limited quality of such sources.The dissemination of accurate cancer screening and prevention information, customized to the population's needs through their preferred information sources should be prioritized, as well as offering more opportunities to increase health/cancer literacy skills'.

Recommendation
As illustrated in the reviews a.Strong public policies are needed that both promote and create awareness of different cancer screening procedures.This includes policies for underserved groups which can benefit from a process of decision making tailored to circumstances that may otherwise prevent the uptake of cancer screening.
'Government and policy makers might revise their strategies to promote screening uptake in other ways [ … ] interventions directed at these levels may help to improve the screening uptake by increasing the facilities available and accessible, supporting childcare, having female physicians speaking the minority's language, and overcoming culturerelated influences that deter screening'. 21b.Policy makers should also consider the role of trust in achieving appropriate uptake of cancer screening.Healthcare providers can capitalize on their trusted influence and join policy makers in designing and delivering appropriate strategies for cancer screening.
'Specifically supported in our findings is the suggestion medical providers capitalize on their influence and join policy makers in efforts to eliminate colorectal cancer screening disparities … ' 14

Recommendation
As illustrated in the reviews a. Future research should consider multimodal or mixed methods approaches that go beyond the clinical setting to reach potential participants who do not currently undergo regular cancer screening.
'Future studies would benefit from a mixed methods approach, including both high quality intervention studies alongside qualitative studies to explore barriers and enablers to screening participation.' 22 b.Further appraisal is needed of current interventions to increase screening uptake (e.g.bowel, breast, and cervical programmes) to assess how the intervention agenda can be revised to better align with inclusive best practices in preventative health.
notably as a 'hot spot' barrier for cervical cancer screening.Potential participants preferred providers who reflected their own lived experiences including aspects such as gender, ethnicity and language. 21,34--36he element of trust was consistent throughout the reviews, including discussions of satisfaction with the quality of care and health services and the overarching facilitator of a healthcare provider recommendation to attend cancer screening.Healthcare providers were typically identified as nurses, general practitioners or primary health care providers, and specialists such as oncologists.The role of a trusted healthcare provider was also reflected in the implications for future research and best practice as recommended by the authors of the included reviews.Recommendations included additional support and training for providers to enhance already existing knowledge of cancer and screening programmes as well as counselling practices for both the wider public and under-served communities.
The need for culturally tailored health promotion was reflected in both barriers and facilitators throughout the reviews.Experiences of discrimination within the healthcare system were noted by five reviews describing differing aspects such as racism, legacies of colonialism and challenges faced by rural communities. 22,32,35,37,38Wider cultural phenomena were also highlighted such as the heteronormative role of masculinity in the acceptability of procedures involving the rectum. 39ulturally tailored health promotion may also be reflected in barriers such as language preferences and/or low levels of health literacy, both of which were noted as contributing to an overall lack of knowledge regarding cancer and cancer screening programmes.Recommendations for future research in this area often overlapped with concepts of prioritizing patient-centred care and patient autonomy.A 'one-size-fits-all' approach to cancer screening fails to consider the heterogeneity within differing cultural traditions. 19,20It was recommended that engagement strategies be designed by and for the individuals within a specific community, focussed on building trust and clear communication with available health services. 19,20stablished examples of such strategies include community-based participatory research and integrated knowledge translation. 40,41hile capturing information about interventions was not part of this overview, the barriers and facilitators presented can further guide discussions on best practices for future research.As evidenced by the reviews there is scope to consider interventions that (i) increase demand for screening services, (ii) reduce barriers to uptake of services and/or (iii) are relevant to the healthcare system and those providing services.The latter also reflects the need to address systemic inequalities through additional measures at the policy level that aim to promote and create awareness of different cancer screening opportunities and procedures.Across reviews, tailored information strategies were described as both barriers and facilitators to screening uptake, with some discussion around the role of media and educational materials that are fit-for-purpose. 18,19,24his overview was not without limitations.By addressing three cancer screening programmes in tandem, a granular assessment of barriers and facilitators was not feasible.We also did not seek an equitable distribution between reviews focussed on barriers vs. facilitators (or a combination thereof).The key factors presented, and the synthesis of future practice recommendations, are intended to provide an overarching reflection on issues that are both unique and common across bowel, breast and/or cervical cancer screening efforts.The depth of barriers and facilitators presented by the included reviews also varied widely in their presentation, with some offering contextual details and others lacking this additional description.Facilitators were comparatively under-researched (or under-reported) and may offer a potential avenue for future research and development.
We sought to identify and discuss the factors influencing uptake of cancer screening programmes and not which groups of people are most or least likely to participate.As with any overview of existing reviews, the search process itself was also limited in its capacity, including the decision to restrict inclusion to reviews published in three key databases, and to only incorporate studies from high-income countries published in English.We sought to balance the thoroughness of the search with the needs of those commissioning the research with regard to the use of time and money.We used the JBI Checklist for Systematic Reviews and Research Syntheses to assess the methodological quality of the included reviews, but we did not attempt to reassess the risk of bias of the individual studies included in each review.Furthermore, we did not quantify the degree of overlap between reviews in terms of included studies.Pre-established frameworks or guiding theories were also not incorporated into the analysis.This overview sought to offer overarching insights for multiple cancer screening programmes, and choosing one framework or theory as a lens for analysis could potentially limit the applicability of the insights.Additional research that is fit-forpurpose within cancer screening programmes is needed to further contextualize the identified factors as they relate to uptake.
In conclusion, this overview acknowledges a need for further informed research design when considering the barriers and facilitators that may influence the uptake of cancer screening programmes.A key recommendation identified within the reviews is to consider multimodal or mixed methods approaches to research that go beyond the clinical setting to reach potential participants who do not currently undergo regular cancer screening. 22There is also a need to further appraise current interventions across programmes to discuss how the intervention agenda can be revised at both local and national levels to better align with inclusive practices in preventative health. 23As shown by the findings of this overview, across all factors 'trust' and 'building trusted relationships' with diverse communities are integral to the success of cancer screening programmes and must be reflective of collaborative efforts to mitigate barriers and enhance facilitators to uptake.

Figure 1
Figure 1 Results of the search process.

Table 1
Barriers to the uptake of cancer screening services Social acceptance Cultural related factors to the social acceptance of screening Lack of support provided by family members and/or social networks Social stigma 12. Trust Distrust in the individual healthcare provider performing the test including gender and ethnic preferences not being met Lack of a recommendation from a healthcare provider to attend screening Lack of culturally competent healthcare Overall dissatisfaction with the quality of care and health services Psychological discomfort during the test itself including feelings such as embarrassment, vulnerability, shame, and/or anxiety Other perceived emotional or psychological barriers to undertaking the screening procedure (not specified) 10.Resources Difficulties navigating the healthcare system including unclear messaging on where to go for screening Distance to testing facilities including concerns about transportation Inadequate access to a regular source of care, including a primary care provider Scheduling issues including forgetting to book/attend appointments, unsuitable appointment times, and time constraints such as work commitment or childcare concerns Shortage of healthcare providers 11.

Table 2
Facilitators to the uptake of cancer screening services Access to a regular source of care, including a primary care provider 8. Social acceptance Acculturation, or the process through which a person or group from one culture comes to adopt the practices and values of another culture Acting as, or following, a role model Support provided by family members and/or social networks 9. Trust Culturally competent healthcare Healthcare provider recommendation to attend screening Low perceived discrimination in the healthcare setting Overall satisfaction with the quality of care and health services Providers who reflect the lived experiences of patients including gender, ethnicity, and language preferences