Optimizing the implementation of lung cancer screening in Scotland: Focus group participant perspectives in the LUNGSCOT study

Abstract Introduction Targeted lung cancer screening is effective in reducing lung cancer and all‐cause mortality according to major trials in the United Kingdom and Europe. However, the best ways of implementing screening in local communities requires an understanding of the population the programme will serve. We undertook a study to explore the views of those potentially eligible for, and to identify potential barriers and facilitators to taking part in, lung screening, to inform the development of a feasibility study. Methods Men and women aged 45–70, living in urban and rural Scotland, and either self‐reported people who smoke or who recently quit, were invited to take part in the study via research agency Taylor McKenzie. Eleven men and 14 women took part in three virtual focus groups exploring their views on lung screening. Focus group transcripts were transcribed and analysed using thematic analysis, assisted by QSR NVivo. Findings Three overarching themes were identified: (1) Knowledge, awareness and acceptability of lung screening, (2) Barriers and facilitators to screening and (3) Promoting screening and implementation ideas. Participants were largely supportive of lung screening in principle and described the importance of the early detection of cancer. Emotional and psychological concerns as well as system‐level and practical issues were discussed as posing barriers and facilitators to lung screening. Conclusions Understanding the views of people potentially eligible for a lung health check can usefully inform the development of a further study to test the feasibility and acceptability of lung screening in Scotland. Patient or Public Contribution The LUNGSCOT study has convened a patient advisory group to advise on all aspects of study development and implementation. Patient representatives commented on the focus group study design, study materials and ethics application, and two representatives read the focus group transcripts.


| INTRODUCTION
Lung cancer remains one of the major causes of cancer mortality globally, and Scotland has high incidence and low survival rates compared with the rest of Europe. [1][2][3][4] Despite many initiatives to raise awareness and encourage early symptomatic presentation, most lung cancers are diagnosed at a late stage, and overall survival is poor. 5 A recent Public Health Scotland report revealed that the Covid-19 pandemic has had a further negative impact on the clinical presentation of lung cancer, with a reduction in diagnoses during the lockdown periods, and an anticipated wave of late diagnoses from this backlog. 6 Over the last 5 years, there has been a growing body of evidence from trials in the United States and continental Europe, and pilot studies in the United Kingdom, demonstrating survival gains from low-dose computed tomography (LDCT) screening for lung cancer in high-risk populations. 7-10 A recent meta-analysis of this evidence provides a strong case for the implementation of targeted lung screening, supported by expert clinical opinion, 11 and the UK National Screening Committee has recently recommended in favour of targeted lung screening. However, there are still many lung screening implementation challenges to be addressed. 12,13 Importantly, lung screening is most effective if targeted at high-risk groups-ideally using validated risk prediction tools to assess who is at the highest risk of developing lung cancer and would most benefit from screening, namely smokers or recent quitters, aged 55-74 years.
To date, UK pilots and trials, including the Early Detection of Cancer of the Lung Scotland (ECLS) trial in Scotland using blood biomarkers to detect early signs of lung cancer, have shown variable and socially patterned uptake of screening, 8,[14][15][16] and work has been done to understand barriers to participation. Uptake remains lower in more marginalized groups-that is, heavy smokers living in more deprived areas. 17 Further research to understand the views of Scotland's population on the acceptability of lung screening, and barriers and facilitators (related to issues of geography, rural and urban deprivation and a high burden of multimorbidity), will help shape future pilots and programmes in Scotland.
This focus group study explores the views of people potentially eligible for lung screening, identifies perceived barriers and facilitators to participation, and examines strategies to optimize the implementation of lung screening in Scotland. It forms part of the LUNGSCOT study, which is examining the feasibility of introducing lung screening in Scotland. 18 CAVERS ET AL. | 3247 2 | METHODS We conducted three focus groups with self-reported 'heavy smokers' living in rural, urban and deprived areas of Scotland to ascertain their views on barriers to lung screening. Focus groups were considered the most appropriate method for engaging with those eligible for screening, as they enabled an understanding of how participants perceive the prospect of lung screening through discussion and they enable the sharing and development of ideas. 19 Findings from the focus groups will feed into the development and design of the lung screening pilot. We employed a range of strategies and reflexive practices to ensure that focus groups were participant-led and datadriven. 20

| Identifying participants
Participants were recruited through Taylor McKenzie (TM), a Scottish-based company that specializes in qualitative research, to identify members of the public eligible to take part in the focus groups (https://www.taylormckenzie.co.uk). TM developed a studyspecific screening questionnaire (further details below) to allow the purposive sampling of eligible participants from their extensive database of people willing to take part in health, social or marketing research.

| Recruitment and sampling
We aimed to recruit up to 24 people from across Scotland to take part in three separate focus groups of 8 people, considered to be an appropriate number to identify a range of views. 21 Interested people responded to recruitment notices posted on TM's mailing list and social media pages. We used the inclusion and exclusion criteria listed In Box 1.
Those who responded were provided with a study information sheet by TM and given 7-14 days to consider taking part. TM drew up a list of eligible participants (based on information on their database, e.g., socioeconomic grade [SEG], occupation, and from speaking to potential participants directly, e.g., smoking status) and added it to a secure portal for the researchers to access and review.
Eligible participants were allocated to a focus group at a preset date and time. Participants were offered a financial reimbursement for their time, paid via TM.

| Focus groups and consent
Three focus groups, lasting approximately 75 min, were run virtually using the online video conferencing platform Zoom, selected due to likely participant familiarity with it, and to comply with the prevailing government restrictions on face-to-face meetings at the time due to the Covid-19 pandemic. Participants were asked to sign a digital consent form via TM ahead of the focus group and verbal consent was agreed upon at the beginning of each focus group. Focus groups were led and facilitated by two researchers (D. C. and M. N.-health services researchers), with one group comprising those living in rural areas and the other two urban groups. Participants did not know one another before the focus group. The format and content of the focus groups were developed by a subgroup of the research team with expertise in behavioural aspects of cancer screening, drawing on relevant literature. The lung screening process was explained to participants: eligible people would be offered a LDCT scan to detect any lung conditions, one of which is lung cancer. The topic guide (see

| Analysis
Focus group recordings were transcribed verbatim and subject to Braun and Clarke's 22 thematic analysis, chosen as it is the most commonly used approach considered appropriate to derive key themes and ideas from the group discussions, taking context into account 19 and consistent with social constructionist underpinnings.
Using thematic analysis allowed us to incorporate guidance specific to focus group interviewing and its impact on analysis, for example, considering dynamics, social comparison and power imbalances within groups. 23,24 Transcripts were read repeatedly and compared and contrasted to develop a set of common codes by D. C. These • Non-English speakers, preventing them from comfortably taking part in a discussion codes were applied back across the data and assigned to excerpts from the focus groups using QSR NVivo version 12 Pro (www. qsrinternational.com) by D. C. and J. R. (a research intern). Codes were further refined and a set of overarching themes and subthemes were inductively derived to interpret and explain the data, in discussion with the wider research team and patient advisory group.
The LUNGSCOT team comprises health services researchers, health psychologists, clinicians, a health economist and patient and carer representatives. Themes were placed in the context of existing literature and theory to incorporate our findings into the wider evidence base.

| Patient advisory group
The patient advisory group was convened for the purpose of the wider LUNGSCOT study. The group comprises three patients and one carer with experience in lung cancer and two patients with other cancers. The group has been involved in the study design and commented on study documentation as well as two advisors reading transcripts and sharing their views on the analysis. The group meets quarterly to discuss study progress and opportunities to get involved in study tasks.

| FINDINGS
Eleven females and 14 males aged 45-70 years living in a mix of urban and rural areas in Scotland took part across the three focus groups.
Eleven participants were current smokers, and 14 had quit within the previous 2 years. All participants were from the lower socio-economic grades (SEG): C2 (skilled manual workers), D (semiskilled and unskilled manual workers) and E (nonworking). Twenty-one participants were White British/Scottish, one person was Black British, one British Asian and one South Asian. All participants had school-level or vocational qualifications but no one had a higher education degree. See Tables 1-3 for participant characteristics.
Our analysis identified three overarching themes in the data: (1) Knowledge, awareness and acceptability of lung screening, (2) Barriers and facilitators to screening and (3) Promoting screening and implementation ideas.

| Knowledge, awareness and acceptability of lung screening
There is currently no national lung screening programme in the Participants said that most people had received smoking cessation advice before, they already knew that smoking was harmful, and would not be offended by a health professional asking them about smoking. There was a strong sense among participants that the desire to quit smoking and action to quit was self-motivated.

| Individual level influences on screening intentions
On an individual level, there were a number of cognitive, psychological and emotional factors influencing screening intentions.

Psychological and emotional concerns
The most pronounced psychological and emotional concerns re-   Having outlined what the screening process would entail, participants did not voluntarily raise any concerns about radiation exposure, over-diagnosis or invasiveness of the LDCT procedure.

| Practical and system barriers
Participants were supportive of a 'proper' check of the lungs, including identification of nodules to be monitored or other incidental findings, particularly when they had existing lung problems.

| Promoting screening and implementation ideas
There was considerable discussion in each focus group on the acceptability and accessibility of screening, leading to suggestions of ways of promoting and implementing screening to increase participation. Participants' views on accessibility were of particular interest due to their socioeconomic status and geographical diversity.
Suggestions related to the cognitive and psychological barriers to screening as well as practical issues.

| Comparison with existing literature and theory
There is a strong consistency in our findings with the growing body of evidence looking at attitudes to screening and screening behaviour, across a range of screening programmes and for lung screening in particular, in the United Kingdom and beyond. [26][27][28] LDCT screening for lung cancer is largely unheard of in Scotland but has a high degree of acceptability more broadly, or among those who have participated in screening. 27,29,30 There was an evident awareness among participants of the benefits of early detection and thus support for lung screening, in line with other research. 17,31 Fear was identified as one of the most common psychological barriers to lung screening, which is reflected in the literature in both survey and qualitative explorations of attitudes to screening. 28,32,33 Linked to this was a sense of fatalism or predicted fatalism among older generations, also mirrored in comparable studies of lung screening. 29,34 While there is evidence to suggest that the fear and anxiety associated with lung screening participation is transient 35 and can be a motivating factor to be screened, quit smoking and even other cancer-preventing health behaviour change, [36][37][38] it is still vital to minimize this emotional response by addressing and managing it.
Positive messaging in the promotion of screening, such as sharing the treatment successes and mortality gains from early detection, is one potential step in approaching this.
Notions of risk were a key component of our group's considerations of whether or not someone would take part in screening, often related to not experiencing symptoms and having stopped smoking.
Perceived risk has been identified widely in the literature to explain decision-making in relation to screening and help-seeking for symptomatic illness. 28,33,39,40 Risk and decision-making are discussed further below.
Perceived judgement and stigma related to smoking featured in focus group discussions. This is widely evident in the literature, along with self-blame. 31,38,41 Stigma has been identified in the literature as a barrier to help-seeking for signs of lung cancer and it seems this also applies to screening participation. 42 Related to this was a sense of fatalism-participants in our study did not consider they would blame themselves if they developed lung cancer, but some did feel that the damage was already done and screening could not change that. 17,29,38 However, this was not a clear barrier. For some, it was a good reason to detect any inevitable lung cancer at an early stage, suggesting that issues such as fear, blame and fatalism are complex and operate on a pendulum when prompting action or inaction.
Discussions of stigma inevitably moved onto smoking cessation. -one example is streamlining procedures to identify high-risk patients from practice data. 7,8 It also seems logical to harness the successes of implementation strategies for other cancer screening (e.g., the UK's bowel screening programmes). 52,53 In addition to the psychosocial issues discussed by focus group participants, practical barriers to participation in lung screening including time, cost, travel and competing work or other commitments, were also mooted. Practical barriers are commonly reported throughout the evidence base related to engaging with screening, with a suggestion that these barriers are heightened in more deprived groups. 27,32,46 Von Wagner et al. 50 have developed a model of screening behaviour, accounting for a range of factors identified in relation to wider health behaviours, such as health identity and self-efficacy, that can be usefully mapped onto the findings of this study. Similarly, Robb 54 has developed the I-SAM model to understand screening participation. Application of these models to follow-up interviews as part of the planned pilot lung screening study in Scotland will be enlightening to confirm the salience of these to screening participation and nonparticipation.
There is an abundance of early cancer detection research exploring how people appraise bodily changes, evaluate risk and decide to seek medical help, as well as conceptual models to understand these processes. [55][56][57] There is also some utility in applying these to screening behaviour, often in the absence of  61 Speaking to people who have taken part in screening or chosen not to take part is also essential to further understand the relationship between intention and behaviour.
We also reflected on the group dynamic together with the nature of our role in conducting the focus groups, and whether this was likely to influence people in agreeing with and supporting the concept of lung screening. However, the open nature of questioning, reminding participants that we genuinely wanted to hear their views, and the self-selecting group of individuals who were quite assured in their own responses, suggested that we did not shape this narrative.

| Implications and future work
This study informs the development of strategies to improve uptake and informed choice in lung screening. It is essential to understand people's health beliefs and behaviours and to target the barriers to implement a patient-centred service using a theory-driven approach. 62 This work adds to a growing evidence base shedding light on the behavioural aspects of screening participation and will inform the design and implementation of a new lung screening pilot in Scotland 40,45,46 (see Box 2 for implementation ideas generated from this work). Minimizing practical barriers is also likely to be instrumental in improving participation and addressing inequity in access to screening. As such, information materials, methods of