“To know or not to know…?” Push and pull in ever smokers lung screening uptake decision‐making intentions

Abstract Background In the United States, lung cancer screening aims to detect cancer early in nonsymptomatic current and former smokers. A lung screening pilot service in an area of high lung cancer incidence in the United Kingdom has been designed based on United States trial evidence. However, our understanding of acceptability and reasons for lung screening uptake or decline in a United Kingdom nontrial context are currently limited. Objective To explore with ever smokers the acceptability of targeted lung screening and uptake decision‐making intentions. Design Qualitative study using semistructured focus groups and inductive thematic analysis to explore acceptability and uptake decision‐making intentions with people of similar characteristics to lung screening eligible individuals. Setting and participants Thirty‐three participants (22 ex‐smokers; 11 smokers) men and women, smokers and ex‐smokers, aged 50‐80 were recruited purposively from community and health settings in Manchester, England. Results Lung screening was widely acceptable to participants. It was seen as offering reassurance about lung health or opportunity for early detection and treatment. Participant's desire to know about their lung health via screening was impacted by perceived benefits; emotions such as worry about a diagnosis and screening tests; practicalities such as accessibility; and smoking‐related issues including perceptions of individual risk and smoking stigma. Discussion Decision making was multifaceted with indications that current smokers faced higher participation barriers than ex‐smokers. Reducing participation barriers through careful service design and provision of decision support information will be important in lung screening programmes to support informed consent and equitable uptake.


| INTRODUC TI ON
Despite fewer people smoking, lung cancer causes nearly 36 000 deaths annually in the United Kingdom (UK) 1 with incidence rates forecast to increase until 2030 due to the ageing population and risk reduction times following smoking quits. 2 How quickly lung cancer is found is strongly linked to survival times. 3 Just 17% of people diagnosed with stage IV lung cancer are alive 12 months later, compared to 83% diagnosed at stage I. 4 Survival rates have not increased much over the last four decades 4 and late-stage diagnosis remains the experience of the majority. 1 Into this gloomy picture has come the results of the National Lung Screening Trial (NLST) 5 in the United States which reported 20% fewer lung cancer deaths following yearly screening with low-dose computerized tomography (LDCT) over 3 years compared to chest X-rays in 53 456 high risk ever smokers. 6 This led to the introduction of lung cancer screening for 55-to 77-year-olds (if smoked for 30 packyears or more and were continuing or stopped within 15 years) 7,8 in the United States and calls for screening to be introduced elsewhere. [9][10][11] Lung cancer screening is not currently approved as a UK wide programme, 12 and questions have been asked about the balance of harms and benefits from being screened. 13 The UK Lung Screening Study (UKLS), a pilot randomized control trial undertaken in the Merseyside and Cambridgeshire areas with smokers and ex-smokers aged 50-75, encouragingly reported 85.7% cancers were diagnosed at stages I or II in its screening arm, but was underpowered to detect mortality impact. 14 UK national policy with regard to lung screening will be reviewed when European lung cancer screening trial results have been pooled. 15 However, in the meantime funding for National Health Service (NHS) lung screening pilots have been announced. 16 It has been suggested that as LDCT scans are quick, painless and identify treatable disease, screening should be publically acceptable, despite some radiation risk. [17][18][19] Indications are that lung screening invitees perceive screening benefits to include gaining early treatment and relief from worry about having lung cancer but not all invitees wish to be screened. [20][21][22] Lung screening is unique amongst cancer screening as it is looking for a disease closely linked with smoking which is strongly stigmatized. 18 Lung screening uptake by smokers, often living in deprived areas, has been identified as a particular challenge. [23][24][25][26][27] Patel et al 18 categorized nonresponders to lung screening as "too old to be bothered," "worriers," "fatalists" or "avoiders". Avoiding finding out if cancer was present, perceptions of personal risk, individual benefits, practical and emotional barriers have all been identified as influences in lung screening uptake decision making. 14,21,22,28 Other studies have reported that current smokers more than ex-smokers consider cancer a "death sentence" expect less benefit from early detection and have higher uptake barriers. 15,17,22,29 Contrastingly, Cataldo 30 reported that older smokers were receptive to lung screening and suggested that further understanding of smokers' views was needed. 15,17,19,22,29 Our understanding of the views of ever smokers about lung screening is currently limited in a UK nontrial context. 14,18 The only other lung screening study exploring the views of ever smokers in UK nontrial context which the authors are aware of found cancer fatalism, low lung health expectations and smoking stigma as uptake barriers. 19 To test the viability of lung screening outside of a research trial context, an NHS pilot screening service has now taken place in Manchester, England. 31 This offered a "lung health check" (risk assessment and spirometry) to current and former smokers aged 55-74, with no lung cancer diagnosis within 5 years and who were not on a primary care palliative care register. Appointments were in mobile facilities in supermarket carparks. An LDCT scan was offered immediately on site for individuals with a 1.51% lung cancer risk or higher in the next 6 years unless they had a chest CT scan within 12  Baseline results from the first scan round were that 80% of lung cancers were found at stages I and II. This was a significant stage change (P < 0.0001) compared to the same area the year before and allowed 89% of people where lung cancer was found to be offered curative intent treatment. 31 Initial findings from this qualitative study (first four focus groups held February to May 2016) informed thinking about the Manchester pilot service design and its patient information materials.

| OBJEC TIVE S
The study objectives were to explore with ever smokers aged 50-80 Targeting refers to the lung screening eligibility criteria based on smoking status, smoking history and age. "Acceptability" was considered as positivity about the service in principle and expressed intent for use.

| Design, setting and participants
We undertook a qualitative study to explore lung screening acceptability and uptake decision making with people of similar characteristics to screening eligible individuals. Qualitative research is a recognized way to explore potential service users views [33][34][35] and assist in translating research to real-world practice. 36 This is important as most lung screening knowledge is from experimental settings. 21 The study setting was Manchester, a "postindustrial" city 37 with significant deprivation, higher lung cancer incidence and lower life expectancies than England averages. 38

| Data collection
Data collection used semistructured focus groups to allow participant interaction to generate understanding. 39,40 To facilitate freer expression and comparison, separate groups for smokers and ex-smokers were held. Six groups (three for smokers and three for ex-smokers) were held in accessible community locations (February to June 2016). It was anticipated that given the study scope, this would provide sufficient data without missing new insights. 41 Each group was mixed by gender, age, ethnicity and address deprivation.
The corresponding author acted as group moderator supported by an assistant moderator. The topic guide included lung screening, lung cancer beliefs and uptake intentions. Groups were audio-recorded, transcribed verbatim and checked for accuracy. Participants were given service information and asked what they would do if they received a screening invite; responses were noted following a show of hands.

| Analysis
To protect anonymity, pseudonyms were used and identifiable information in transcripts extracted before uploading into computer software N-Vivo 11 with characteristic information and address deprivation from postcodes matched to Indices of Multiple Deprivation levels. 42 Inductive thematic analysis 43 was chosen to identify themes within data rather than use pre-existing literature concepts. 44 Analysis used Braun and Clarke's recommended steps for thematic analysis 43 and was completed separately for smoking and ex-smoking groups. This commenced with data familiarization (listening to recordings and rereading transcripts). Early codes were identified, added to transcript sections and reread to identify groups of similar comments by the corresponding author. A description of early categories was written and the data checked for correct inclusion by the corresponding author. Discussion about the categories was held between the corresponding author and assistant moderator. Initial themes 43 were identified by the corresponding author who considered categorized data to see what patterns and linkages existed and discussed between an independent researcher and the corresponding author. Theme identification and interpretation were assisted by "writing memos", "diagramming" 45 and asking questions about significance, underpinning influences and implications. 43 Participant characteristics were also considered to identify any patterns and linkages.
Refinements were made by consensus until a final "thematic map" was considered appropriate. 43 Theme saturation was considered to have taken place when additional data did not add new information and theme explanations made sense to the corresponding author and assistant moderator. Analysis after four groups was compared with that from the final two groups to indicate when sufficient data had been collected. Writing up included illustrative participants' quotes and discordant data. 46
Participants included men and women with mixed ages (age range: 50-80) and socioeconomic backgrounds. Employment status varied; around half were retired. The majority were ex-smokers and of white ethnicity. There were more male current smokers than female (eight men; three women). Over two-thirds knew someone who had had cancer, around a third for lung cancer. Demographic characteristics of participants are shown in Table 1 below.
While nearly all participants were supportive of lung screening as an idea, many participants expressed a dilemma about whether to be screened if the opportunity arose. Two main themes were found:

| Theme one: acceptability
This theme is about the acceptability of lung screening. Lung screening as a general idea was found to be widely acceptable and strongly welcomed by nearly all participants. Many participants talked about smoking and coughing as an indication that lung health was generally poor for them, their family or friends. Several recounted experiences of family and friends with lung cancer dying quickly following diagnosis.
Oh, I think it's a very good idea because I have two brothers who -well we all grew up in a family of smokers and beyond that even grandparents andbut -well both my brothers live near x anyway so that would be good and they're still smoking and terrible coughs. In fact their dad, actually their dad died of lung cancer but he'd smoked from 12 to 82 and that wasn't the only thing that was on his death certificate. It was like pneumonia and -I'm not that bothered about myself even though I smoked but listening to them coughing, it's awful, just like their dad, he coughed all his life really and my life.

Female6ExsmokerFG2
In this context, lung screening was conceptualized as "an early warning system" (Male1SmokerFG4, Male6SmokerFG6) and a way to stay well in older age. Having your lungs checked via screening was considered a logical approach based on general screening knowledge related to established screening programmes for other diseases rather than lung screening specifically.
It's like the bowel screening programme thing, like that. It's got to be beneficial hasn't it?

Male4ExsmokerFG1
Many participants were so enthused by the idea of lung screening that they felt the eligibility criteria, which were generally viewed as cost-limiting measures, should be broadened to include older and younger people. It was generally accepted that a screening service was needed by smokers and ex-smokers. Concerns were raised in most groups about excluding others considered to be at risk, such as passive smokers and people exposed to industrial and environmental pollutants.
In terms of broadening the group, first of all, some heavy smokers are diagnosed with lung cancer before the age of 50. So, going further down, so from maybe 45, if it could be afforded it might be a

| Subtheme three: practicalities
Simple practicalities (location, booking speed and appointment availability) were identified as barriers to lung screening uptake by many participants. For participants with positive, but tentative uptake in- Many participants talked about screening as revealing the personal impact of smoking and one suggested screening uptake required taking personal responsibly for a health-damaging habit. A few participants suggested that as smokers, they would be treated less sympathetically by medical professionals should lung cancer be found.
It's you, it's a personal -why, the consequence of you smoking. But you know that every time you took a cigarette out the packet; you knew it's detrimental to your health. So now we're going to find out proper, knock on the head, it was you and all them years taking responsibility for your consequences.

Female2ExsmokerFG1
I think that if you're a smoker or an ex-smoker a lot of doctors treat you like you're a leper. It's a dirty disease because you smoke. Female5ExsmokerFG2 For some, mainly ex-smokers, lung screening was viewed as part of pursuing healthier habits. Smoking cessation was not extensively discussed; however, a few current smokers indicated a diagnosis would prompt quitting, and others felt an all-clear would suggest they still had chance to improve their lung health through quitting.

| Multifaceted decision making
There were multiple influences on participants' uptake decisionmaking intentions. This aligns with others findings 18-20 as did the reasons why some participants expressed a preference for screening (early diagnosis and potential reassurance) and some did not (lung cancer diagnosis fear and low levels of perceived personal benefit). [17][18][19]22,29 Other studies have also found that waiting for results and hospital attendance created anxiety 19,21,30 and were participation barriers. 18,21 However, there were differences with some of the literature. In this study, while some participants expressed fatalism and did not feel they would benefit due to low lung health expectations and limited belief in treatment effectiveness, this was not as widespread as indicated for London's deprived area smokers. 19 Many participants in our study expressed keenness to be screened as this could result in finding lung cancer early and increase survival chances. This is more in line with Cataldo's findings 30 and may relate to this study's more socioeconomically mixed sample or it is possible that as the researchers were NHS employed with study participation invitations arising from an NHS organization this may have reduced negative comments. This was mitigated through building rapport with participants, the topic guide and seeking alternative views; however, the researcher's influence cannot be discounted. 47

| Emotional barriers
In our study, the preference not to be screened was strongly linked to a fear of being diagnosed with lung cancer as has been found elsewhere. 18,19,21,22 Cancer worry was reported as an uptake barrier in the UKLS for current smokers, women and people from more deprived areas where widespread negative experiences of lung cancer may generate more pessimistic attitudes. 21,48 In this study, we also found that anxiety about personal disease risk motivated screening uptake for some participants. The desire for "reassurance" via lung screening has been found elsewhere [17][18][19] including in other screening programmes where worry has been reported as motivational for some and a barrier for others. 25 In view of the influence of worry on lung screening uptake, the communication of survivorship stories, information about effective treatments and screening tests may help reduce fear barriers.

| Smoking
In this study, similar proportions of smokers and ex-smokers expressed positive screening intent in response to viewing sample invitational materials. However, some differences were indicated.
When asked what they would do with an invite letter, ex-smokers expressed more definite positive screening intentions than current smokers whose views appeared more tentative. Current smokers also commonly talked about how other's needed screening more than they did, due heavier smoking or worse symptoms and emphasized pollution-related lung cancer causation. This suggested personal smoking risks and screening need was being downplayed.
However, some of these same participants were also extremely worried about a cancer diagnosis. This was so high for some, especially current smokers, that they felt cancer would almost inevitably be found if they were screened-as has been reported elsewhere. 19 This seeming contradiction supports Quaife et al's 49 view that smokers experience "cognitive dissonance" 50 about continuing to smoke while knowing its risks. It has been suggested that this results in biased thought processing 51-55 distorting risks in "defensive denial", 56 not wanting to be faced with risk information, such as would be apparent from attending lung screening. [17][18][19]22,49,57 The indication in this study that lung screening uptake required facing-up to smoking consequences supports this. In fact, "avoiders" were one of Patel's nonresponder types. 18 However, this finding is tentatively presented as there were fewer current smokers (11 smokers; 22 ex-smokers) and a lower number of female current smokers (three women; eight men) than planned due to participant drop out which limits these findings. We also need to consider that smokers are not a homogenous group and lung screening views may also vary with socioeconomic status 28 and other factors. For example, Hahn 58 reported that screening interest varies with quit intention with smokers actively considering quitting more interested than others.

| An Informed choice?
Screening participation should be an "informed choice", 59 Our study's participants commented that a decision to participate, or not, in lung screening was their choice, but to be an "informed choice," improved participant knowledge is needed. 17,19,62,63 In the United States, joint discussions between patients and health care providers have been mandated by Medicare in the lung screening process to support informed decision making. 64 Supporting informed and equitable lung screening uptake is an anticipated challenge in the UK. 65 further testing is needed. 76,81 In the UK, there are currently no guidelines for developing quality assured lung screening patient literature or established decision-making tools. Future research could usefully consider the feasibility and impact of lung screening decision aids in a UK context.

| Push and pull in decision making
The desire to know about personal lung health in this study was influenced by participant's views about benefits; emotions; smoking; and practicalities. These appeared to motivate uptake for some participants but were a barrier for others. For example, the anticipation that a lung health check would result in personal health benefit encouraged uptake, but low benefit expectations discouraged attendance. Worry could either encourage lung screening or was an obstacle. Practicalities about service access-their ease or difficulty acted similarly. Smoking was a barrier to uptake where health risks were downplayed or where stigma was felt, but was motivational when risks were recognized and faced. Figure 1 below illustrates this "push and pull" effect on uptake decision-making intentions pictorially. This is important as it indicates points where public health action and careful service design could minimize participation barriers. Practice-based actions are suggested in Figure 1 relating to the theme "desire to know about personal lung health". This draws on the experience of the Manchester NHS lung screening pilot which has recently reported its baseline findings. 31

| Study strengths and limitations
Our study is useful to build understanding as lung screening pilots are now being developed in the NHS 31 and adds to the limited UK evidence base outside of a trial context. However, these findings should be considered limited by sample make-up and context 47 in this case a postindustrial city 37 with high incidence lung cancer and deprivation. 38,82 Given the relatively small purposive sample, it is also possible that participants may have different views to the wider population and that invitations from an NHS organization to participate may have reduced expression of some negative screening opinions. Focus group discussions sparked conversations revealing insights but may have concentrated opinions. 83 Alternative views were sought, discordant data included and separate groups for current and ex-smokers allowed free expression of views. The final two groups did not produce additional themes, but confirmed those found previously.

| CON CLUS ION
This study suggests that lung screening was widely acceptable and welcomed by participants with similar characteristics to the screening target group. The desire to know about personal lung health was influenced by emotions; benefit views; practicalities; and smoking. Current smokers appeared to have higher uptake barriers than ex-smokers and tackling this will be a key challenge in lung screening programmes. Some barriers can be addressed at the service level for which recommendations have been made. Future research could helpfully explore the effectiveness of different types of informational materials in supporting "informed participation" and the views of smokers further. Lung health checks have the potential to open up early treatment benefits to a high cancer risk group and reduce health inequalities. However, this will only be possible if consideration is given to reducing the identified barriers in future lung screening programmes. Commissioning, for administration support. Significant thanks are also given to Dr Cathy Brennan, University of Leeds, for advice on the study design and early analysis and to Dr Jo Ellins, University of Birmingham, for analytic advice and manuscript comments.