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General gynaecology

DOI: 10.1111/j.1471-0528.2011.03030.x www.bjog.org

Exploring age differences in reasons for nonattendance for cervical screening: a qualitative study J Waller,a M Jackowska,b L Marlow,a J Wardlea a Cancer Research UK Health Behaviour Research Centre and b Psychobiology Group, Department of Epidemiology and Public Health, UCL, London, UK Correspondence: Dr J Waller, Cancer Research UK Health Behaviour Research Centre, Department of Epidemiology and Public Health, UCL, 1–19 Torrington Place, London WC1E 6BT, UK. Email [email protected]

Accepted 26 April 2011. Published Online 14 June 2011.

Objectives To explore differences in barriers to attendance at

cervical screening across age groups because coverage of the cervical screening programme in England has been falling, particularly among women in the youngest age group (25– 29 years). Design A qualitative study. Setting A university in London. Sample Professionals working in the screening field (n = 12) and women of varying ages who had either never attended for cervical screening or did not attend regularly (n = 46). Methods In Study 1 we interviewed professionals to elicit their

views on the reasons for lower screening attendance in young women. In Study 2, we carried out four focus groups (n = 27) and 19 individual interviews with under-screened women to explore their barriers to attendance. Verbatim transcripts were analysed using Framework Analysis.

Results Reasons for nonattendance were many and varied. Health professionals identified population-level factors, service provision issues, time pressures, risk perceptions, lack of knowledge and psychological barriers. The nonattenders fell into two groups: those who had made an active decision not to take part (who tended to be older), and those who intended to be screened but did not attend (predominantly younger women). Practical barriers were raised more often by younger women whereas older women had more negative attitudes to screening. Conclusion This study provides rich data on the complex reasons

why women do not attend for cervical screening. It points to age differences in barriers to screening, and suggests that addressing practical issues such as appointment systems and clinic times may have a positive impact on attendance in young women. Keywords Barriers, decision-making, papanicolaou test, psycho-

logical, screening coverage, uptake.

Please cite this paper as: Waller J, Jackowska M, Marlow L, Wardle J. Exploring age differences in reasons for nonattendance for cervical screening: a qualitative study. BJOG 2012;119:26–32.

Introduction Women in England are invited to attend for cervical screening every 3 years from age 25 to 49 years and every 5 years from age 50 to 64 years. Since the introduction of the call–recall programme in 1988, coverage has been around 80%.1 However, in recent years coverage has been declining,2 especially in the youngest age group. The latest figures suggest that only two-thirds of 25–29-year-olds in England have been screened within the last 5 years; down from 75% in 2001.2 Similar trends have been noted in other countries including Australia, Canada, Sweden, Denmark, France and Italy.3 Because the incidence of cervi-

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cal cancer is highest in women in their thirties,4 nonattendance for screening in young women has the potential to lead to diagnosis at a later stage of cancer and to poorer outcomes. Few studies have examined age differences in screening attendance or explored the reasons that young women give for lack of participation. Some authors have suggested a cohort effect, hypothesising that nonattendance reflects broader social disillusionment.5,6 Others have suggested that young women experience more barriers to attendance, such as embarrassment,7 lower perceived risk,8 difficulties with appointment times,9 or not being registered with a GP.10

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Age differences in barriers to cervical screening

The present study used qualitative methods to gain two perspectives on nonattendance for cervical screening, first from professionals working in screening and second from women who do not regularly attend screening. We used interviews and focus groups to gain a richer understanding of women’s decision-making about screening than would be possible with survey data. Qualitative methods allow an in-depth exploration of issues raised by the participants that may not have been foreseen.

Methods Study 1 Interviews (three face-to-face, 12 telephone) were carried out with professionals working in the screening programme and related charities, focusing on their perceptions of screening nonattendance and their explanations for age differences (see Table 1 for sample details). Participants were recruited via the UK Clinical Research Network, the Greater London Primary Care Research Network, and contacts of the research team. Participants were based in London (n = 12) and Bristol (n = 3). Interviews were structured around a topic guide and carried out by MJ and JoW. All except one were recorded and transcribed verbatim; with analysis of the non-recorded interview based on notes taken by the interviewer. Participants gave either written or verbal consent.

Study 2 Women who had never attended for screening, or were irregular attenders, were recruited through a market research recruitment database to take part in focus groups. The database is maintained by Saros (www.saros-researchrecruitment.com/) and participants were recruited and screened for eligibility by the company via email or phone.

Three of the groups were with young women (Focus Groups [FGs] 1–3; aged 25–37 years) and one with older women (FG4; aged 41–64 years) (see Table 2). In addition, 19 women took part in interviews (three by telephone; the rest face-to-face). Four participants were recruited from a previous survey study,6 and the rest via an email to academic and nonacademic university staff. Women were purposively sampled to reflect a range of age groups and ethnic backgrounds (see Table 2). Focus groups and interviews were structured around a topic guide developed with reference to the literature and the study aims, which included past screening experience and perceived barriers to past and future screening participation. As a result of problems with recording equipment, analysis of two groups is based partly on notes but the other FGs and interviews were recorded and transcribed verbatim. Interviews and FGs were carried out by MJ and JoW. All participants gave written consent and were given an incentive payment of £25 to cover travel and childcare costs. The studies were approved by the UCL Research Ethics Committee and the Camden & Islington Community Local Research Ethics Committee and took place in spring/summer 2009.

Analysis After familiarisation with transcripts and notes, a separate thematic framework was developed for each of the three substudies, following the principles of Framework Analysis.11 This allowed us to organise the data systematically and identify barriers to screening. Associations within the

Table 2. Sample characteristics for Study 2 (Nonattenders) Focus groups Interviews

Table 1. Sample characteristics for Study 1 (Professionals; interviews) Profession Practice nurse/nurse practitioner General practitioner GP practice manager GP administrator/receptionist Screening commissioner Cervical cancer charity representative Sex Male Female Age (years) 30–39 40–49 50–59

4 4 2 3 1 1 5 10 3 5 7

Age (years) 25–29 30–34 35–39 40–49 50 and over Ethnic group White Asian/Asian British Black/Black British Mixed race Chinese Unknown Screening history Never screened Currently overdue Up to date but has delayed in the past

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17 2 1 5 2

5 3 3 5 3

15 5 4 2 0 1

14 2 1 1 1 0

20 6 1

6 11 2

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data were explored with a particular focus on possible differences between age groups and reasons for any such differences.

Results Study 1 Seven themes emerged from the professionals’ discussion of screening barriers in young women.

Population-level factors Mobility was thought to be a problem, particularly in London, with young women moving house frequently, and not always registering with a GP because they had little need for healthcare: ‘I think it’s the fact that there’s high mobility and they don’t get the … reminder letters, because they’ve moved’ (P4, practice nurse). It was also suggested that the trend towards having children later could mean that young women were less likely to be reminded opportunistically about screening. Service provision There was a belief that GPs may not always be proactive about reminding women to have screening, and this could be because of changes in the way high coverage is incentivised. One GP acknowledged a tendency to focus on issues included in the Quality Outcomes Framework (which is a reward and incentive programme for GPs in England, including 134 achievement indicators across a broad range of domains; see www.qof.ic.nhs.uk/): ‘As GPs, we’re trying to do a hundred different things … and you tend to do the ones that there are incentives about’ (P7, GP). It was suggested that changing the screening age to 25 years could also have affected uptake: ‘when you’re no longer calling them till their 25th birthday it automatically means … they’re going to come in after 1 or 2 years, whenever they feel like it, that your coverage in that age group (25–29) will be lower’ (P10, screening commissioner). Respondents also talked about the fact that screening is less available at family planning clinics and well-woman clinics than it used to be, which could make it less convenient for women to be screened. Time pressure Many respondents believed that young women were particularly busy, making it difficult to arrange time for screening: ‘if you’re working, if you’re that age, normally people have very busy lives’ (P11, practice manager). Some thought that having children was a barrier to participation, whereas others believed that women with children were more likely to visit their GP surgery and so had greater opportunity for screening. There were conflicting views about whether more should be done to extend opening hours: some described

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the success of evening or Saturday clinics, whereas others found that they made little difference.

Perceived risk and attitudes to health There was a widely held view that young women do not feel at risk of cervical cancer, they feel that screening is irrelevant to them (particularly as many believe the test is for cancer) and health is not a priority at this age: ‘Their health is sometimes at the lower end of the scale … and maybe cervical screening is just not seen as a priority’ (P8, practice nurse). This pervasive attitude was thought to contribute to a ‘lack of peer group pressure’ (P14, GP) to be screened. One practice nurse also mentioned that some young women choose not to be screened because they are not sexually active and feel at low risk. Information and knowledge The professionals believed that young women were poorly informed about cervical cancer and the purpose of screening. Several cited the ‘Jade Goody Effect’ as evidence that raising awareness increases uptake: ‘A lot of patients … thought, oh, cervical smear ... they always thought it could affect the elderly; it’s not the young. And Jade Goody is a young mum’ (P3, practice administrator). (Jade Goody was a high-profile reality TV personality who was diagnosed with cervical cancer in September 2008 and died in March 2009. Her illness received very wide media coverage in the UK at the time of the current study.) There was a perceived need for more publicity about cervical cancer, and education in schools. Psychological barriers There was little evidence that professionals thought that psychological barriers were more prevalent in younger women. However, one practice nurse believed that fear was a significant factor, often associated with having heard stories from friends about abnormal results. Worry about pain was also mentioned: ‘the younger ones that may have never had it done before are worried that it’s painful’ (P2, GP receptionist). Paternalistic attitudes A latent theme emerged, in the form of paternalistic and sometimes coercive attitudes towards encouraging women to take part in screening. This was more common among practice nurses and receptionists than GPs, and though undoubtedly well-intentioned, it indicates that women’s concerns about screening may not always be adequately acknowledged. Encouraging women to take part may be given more weight than ensuring informed participation: ‘It is for their own good and they just don’t want to do it’ (P2, GP receptionist) and ‘They will still seem to have it done if you coerce them enough into having it done’ (P8,

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practice nurse). It is possible that these kinds of attitudes among professionals could make some women feel unable to make an informed choice about participation.

Study 2 Two patterns of nonattendance emerged from women’s own accounts: making an active decision not to attend (disinclined abstainers), and believing in the importance of screening but not translating positive screening intentions into action (inclined abstainers).

Disinclined abstainers The main reason for actively deciding not to have screening was not being sexually active: ‘I’ve always related it to being sexually active, so if you’re not then you’re not at risk whatsoever’ (FG3). Some of these women complained that they had been unable to opt out of receiving screening invitations. The younger women in this group sometimes expressed an intention to have screening when they became sexually active. Others felt that they had weighed up the benefits and potential harms of screening and made an informed choice not to attend. Harms described included repeat tests for low-grade abnormalities: ‘I just don’t want to get trapped in that loop … of going again and again’ (I16, age 32). Less commonly, the decision seemed to be based on misconception: ‘I still feel that if there’s no symptoms you don’t need to worry particularly’ (I4, age 43; where I4 refers to individual interview number 4. [Where quotes are from focus groups, the first initial of the participant is given {if identifiable from the transcript} with the number of the focus group. The individual ages of the focus group participants are not available.]). Inclined abstainers Many women were positively disposed towards screening but did not attend for a variety of reasons, some of which were similar to those described by the professionals in Study 1. Service provision issues were frequently mentioned, particularly difficulties making appointments to fit around other commitments and menstrual cycle (see quote from I7 in the ‘Age differences’ section below). The test itself was often talked about in negative terms. Some women described feelings of extreme embarrassment, violation or pain. There was widespread dislike of the speculum and the test was described as ‘not something that you can particularly want to do’ (I8, age 28). Some women described upsetting experiences, including bleeding after the test (I5, age 44), or being told that their cervix was in a ‘strange place’ (I19, age 56). Apathy was a common theme, with women saying they tended to ‘put off’ making an appointment. As suggested

in Study 1, women said that screening did not seem ‘that vital’ (I8, age 28) and there was a tendency to procrastinate. In some women, media coverage of Jade Goody’s death had heightened awareness of the importance of screening: ‘the Jade Goody thing is making me think more about it because she’s … so close to my age’ (G, FG1). Competing time demands were discussed, particularly by women who were working or looking after children. Screening was listed among a host of other things that needed to be done, and often it dropped to the bottom of the list because is did not seem important or was difficult to organise: ‘I’ve got to have blood tests, I’ve got to go to the dentist, I’ve got to get my hair cut, so what’s low in priority, and a cervical smear test would be right down there I think’ (E, FG1). Low-risk perceptions sometimes contributed to women’s nonattendance, giving them an excuse to put off doing something that they found unpleasant: ‘I think it was bad experience in the past, which then led to apathy and … looking for a way out of going through it again, which was the fact that I didn’t think I was high risk’ (I14, age 49).

Interactions between barriers Complex interactions between reasons for not attending can be conceptualised within the framework of the Health Belief Model12 (see Figure 1). A variety of demographic and psychological factors contribute to the decision about whether to attend for screening. Once an intention has been formed, additional factors including practical barriers can impede the translation of intention into behaviour. Uncertainty about reasons for nonattendance Some women identified possible barriers without being sure whether they really played a role. For example, one woman reported having had a miscarriage shortly after a screening test. She considered whether this was the reason she had not continued to attend regularly: ‘The last test that I actually had done … I was actually pregnant … and towards the end of that month I did actually have quite an early miscarriage, and I was thinking it was the memory of that … is that stopping me from going?’ (I10, age 39). Other women simply said that they could not identify a ‘main reason’ for their nonattendance: ‘I’m not sure what the one reason is’ (E, FG1). Age differences Several age-related trends emerged. Women in their fifties seemed less likely to mention difficulties in arranging an appointment or finding time for screening. They were more likely to cite low levels of worry about cervical cancer or low perceived risk. One woman described how her feelings had changed as she got older: ‘I think it’s as I became more uncomfortable within myself, and as I put on more weight,

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Individual perceptions

Perceived susceptibility to cervical cancer (often low because of sexual history or young age) Perceived severity of cervical cancer (likely ceiling effect)

Modifying factors

Demographic variables Sexual history Sexuality Screening experience Work status Children Registration with GP

Perceived threat (often seen as low, particularly in young women)

Intention formation

Action

Perceived benefits Few immediate benefits Screening prevents cancer in the long term Perceived barriers Procedural (pain/embarrassment) Fear of the result Negative past experience

Cues to action Invitation letters GP recommendation Partner/friend Media (Jade Goody)

Intention to be screened

Practical barriers to attendance Access (appointment times) Time pressure (work, childcare) Other priorities

Screening attendance

Figure 1. Predictors of screening attendance using a Health Belief Model framework.

and as I felt more inhibited, and I didn’t feel comfortable with doctors and I didn’t want anything invasive’ (PA, FG4). Others cited embarrassment and fear of pain, sometimes resulting from previous experiences: ‘I don’t like the metal thingamajig they use actually. I think that’s what puts me off more than anything’ (I6, age 50). Their beliefs often seemed entrenched and they rarely stated any intention to attend in the future. Women in their twenties and thirties were more likely to mention competing demands on their time: ‘it’s … one of those things I keep meaning to do and never quite getting round to doing it, and also I’m aware that when I do actually make the appointment I’m going to have to sort out childcare’ (I10, age 39). In addition, young women talked about having to have an appointment that fitted in with their menstrual cycle, and at times GP appointment systems made this difficult: ‘I did try and make an appointment, but it was very difficult … I had to phone again on the first day of my cycle … I either didn’t remember to phone or, and it was difficult to get through to the GP, and so I never managed to get a test done’ (I7, age 29). Many young women were positively disposed towards screening and for some, having the opportunity to talk about the barriers during a focus group seemed to strengthen their resolve to attend: ‘It’s actually made me feel a bit pathetic, actually, about saying it’s inconvenient for me to go’ (G, FG1).

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Discussion To our knowledge, this is the first study aimed at exploring differences in barriers to cervical screening between women of different ages. We used qualitative methods to identify important themes, and gain insight into the often complex interactions between barriers. The study benefited from the inclusion of health professionals and screening nonattenders to give two perspectives on the issue and highlight service-delivery factors as well as individual barriers to attendance. The barriers we identified included many that have been described before: appointment times, embarrassment, fear of pain, low perceptions of risk, and not prioritising screening.9,13–15 In addition, the health professionals suggested that population mobility, particularly in young women, might be a problem, and some thought that structural factors such as GP incentivisation and the change in the age of first screening might contribute to declining participation in this group; barriers that women themselves would not necessarily be aware of. For some women, the decision not to attend screening was informed; they perceived that the costs outweighed the benefits or they were not sexually active. Although some of the health professionals believed that women lack knowledge and awareness of screening, this did not appear to be the case among the women we spoke to. We also found little evidence for

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the suggestion that nonattendance in young women is part of more general disillusionment.5 Most were motivated to attend but did not carry through their intentions, consistent with previous work on ‘inclined abstainers’.16 Any association with disillusionment may be explained by competing demands on time, rather than underlying beliefs or values. Our study goes beyond much of the previous research in the field, showing how interactions between different types of barriers to screening can be complex. Figure 1 illustrates how these might be conceptualised within the framework of the Health Belief Model.12 The finding that some women were uncertain why they did not attend is important and raises questions about the validity of survey studies that ask women to choose reasons for nonattendance from a check-list. This methodology assumes that women have well-articulated reasons for nonattendance that can be accessed by a simple question. It appears that this is not always the case. As highlighted by our previous work,6 women who attend regularly for screening are just as likely to regard the test as embarrassing as those who do not. There is a need for innovative methods to further understand screening decisions without relying on self-report, e.g. with discrete choice experiments.17 In young women, among whom coverage is most problematic, practical barriers were frequently cited. They appeared to hold positive attitudes to screening but had difficulty finding time, and negotiating appointment systems. This is consistent with previous findings that practical barriers could be more important than emotional ones6,18 and suggests that adjusting service-related factors could improve uptake in this group. Health psychologists have long been aware of this so-called ‘intention–behaviour gap’19 and our study suggests that removing practical barriers and providing cues to action, such as advertisement campaigns, are two ways in which this might be addressed in the cervical screening context (see Figure 1). Future research might consider evaluating text message reminders, drop-in clinics, or making screening available close to women’s work places to make it more convenient. Study 1 suggests that it may also be fruitful to review the way in which GP incentivisation is organised. The inherent tension between ensuring informed choice and maximising participation means that incentivising high coverage can lead to well-intentioned but inappropriate pressure being placed on individual women to encourage them to be screened. The impact that Jade Goody’s death had on screening attendance20 indicates that there are still gains to be made from increasing awareness of cervical cancer or at least of the screening programme and how to access it. A similar phenomenon was observed when Katie Couric21 (an American news anchorperson) had a colonoscopy on live television, leading to an increase in uptake of colonoscopy in

the USA. Raising awareness of screening via a large-scale advertising campaign might replicate the impact of these naturally occurring, high-profile media events. Our finding that older women seemed more entrenched in their decision not to attend for screening is consistent with a study of enhanced screening invitations for nonattenders with a mean age of 53 years, in which only a very small percentage of women attended for screening following a telephone call, or an invitation endorsed by a celebrity or screening commissioner.22 Alternative approaches are needed to ensure that older women are making informed choices where they decide not to attend. Research in women from different countries with different screening programmes is needed to understand the extent to which these findings will apply beyond the UK. Young women seem less likely to attend for screening in several other countries3 but they are more likely than older women to be screened in the USA.23 Given that Canada and the USA have similar opportunistic screening, it is likely that the reasons for the difference in the pattern of attendance across age groups are complex. The study had a number of limitations. All the fieldwork was carried out in urban areas, and the women who took part either lived or worked in London. More work is needed to investigate barriers to attendance among young women in suburban and rural areas. There is also an urgent need to develop innovative methods to recruit women from socially deprived and other ‘hard to reach’ groups whose reasons for nonattendance may be different from those in this study, and who are likely to be at greatest risk of cervical cancer. The study identified a range of themes and possible associations, but larger-scale work is warranted to see whether the tentative age differences identified are robust, and whether they explain patterns of attendance by age in other countries.

Conclusion Different barriers to cervical screening participation appear to be important at different ages. Whereas younger women reported practical barriers, older women cited low levels of worry about cervical cancer or low perceived risk as reasons for not attending. Age-tailored approaches are needed to reduce barriers to screening participation. There is also a need for innovative and subtle methods of understanding women’s reasons for not participating in cervical screening.

Disclosure of interests None.

Contribution to authorship JoW and JaW designed the study and obtained funding. JoW and MJ developed the study materials and carried out

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the data collection. JoW and MJ developed the thematic framework for the analysis. All the authors contributed to the data analysis and drafting of the paper.

Details of ethics approval The studies were approved by the UCL Research Ethics Committee (ref: 1684/001; approved 26 November 2008) and the Camden & Islington Community Local Research Ethics Committee (ref: 08/H0722/108; approved 19 December 2008).

Funding The study was funded by a small grant from Cancer Research UK’s Prevention and Public Health Policy Advisory Group (C7492/A9845), which covered MJ’s salary and the project running costs. JaW and JoW are funded on a Cancer Research UK programme grant. LM is funded by a Cancer Research UK postdoctoral fellowship.

Acknowledgements We are grateful to all the study participants. j

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