“Whilst you are here…” Acceptability of providing advice about screening and early detection of other cancers as part of the breast cancer screening programme

Abstract Objectives This research aimed to assess women's willingness to receive advice about cervical and bowel cancer screening participation and advice on cancer symptom awareness when attending breast cancer screening. Methods Women (n = 322) aged 60–64 years, living in the United Kingdom, who had previously taken part in breast cancer screening were recruited via a market research panel. They completed an online survey assessing willingness to receive advice, the potential impact of advice on breast screening participation, prospective acceptability and preferences for mode and timing of advice. Results Most women would be willing to receive information about cervical (86%) and bowel cancer screening (90%) and early symptoms of other cancers (92%) at a breast cancer screening appointment. Those who were not up to date with cervical cancer screening were less willing. Prospective acceptability was high for all three forms of advice and was associated with willingness to receive advice. Women would prefer to receive advice through a leaflet (41%) or discussion with the mammographer (30%) either before the appointment (27%), at the appointment (44%) or with their results (22%). Conclusions While there is high willingness and high acceptability towards using breast cancer screening as a teachable moment for advice about prevention and early detection of other cancers, some women find it unacceptable and this may reduce their likelihood of attending a breast screening appointment. Patient or Public Contribution This study focused on gaining women's insights into potential future initiatives to encourage screening and early diagnosis of cancer. Members of the public were also involved in piloting the questionnaire.


| INTRODUCTION
Diagnosis of cancer at an early stage is one of the main determinants of prognosis. In England, when breast cancer is detected at an early stage, the 5-year survival rate approaches 98%. In contrast, women who are diagnosed with advanced-stage breast cancer have a 26% five-year survival rate. 1,2 For cervical and bowel cancer, the 5-year survival rate for early-stage disease is also over 90%, but reduces to below 20% for those with advanced-stage disease. [2][3][4][5] It is therefore imperative to detect cancer early for more successful outcomes.
One means of prevention and early detection of cancer is participation in screening programmes to detect asymptomatic cancer or precancer. Another is raising awareness and encouraging timely help-seeking for those with symptoms. In England, the majority of cancers are diagnosed via presentation with symptoms (80%) rather than through screening (6%). 6 Therefore, ways to promote both screening uptake and timely symptom presentation are required.
In the United Kingdom, screening programmes exist for breast, cervical and bowel cancer. For breast cancer, women aged 50-70 years are invited to undergo an X-ray of the breasts (mammogram) every 3 years. Cervical cancer screening is targeted at women aged 25-64 years. Women are initially invited every 3 years, and then every 5 years from age 50. Cervical screening originally involved a Pap smear with cytology testing. More recently, this has moved to initial human papillomavirus (HPV) testing with cytology triage for those who are HPV positive. Bowel cancer screening is offered to all adults aged 60-74 years (50-74 in Scotland) and requires a stool sample every 2 years (initially this involved guaiac faecal occult blood testing, but now uses a faecal immunochemical test). Previously, flexible sigmoidoscopy ('bowel scope') screening was offered at age 55 years, but this is no longer included in the NHS bowel cancer screening programme. The uptake of cancer screening is variable, with the lowest uptake for bowel cancer screening. Although it is higher for breast and cervical screening, coverage has been decreasing over time. [7][8][9] A recent study investigated how many women aged 60-65 years (the only group eligible for all three cancer screening programmes in England) participated in all three during their last invitation round. 10 The study revealed that although 90% participated in at least one screening programme, only 35% attended all three. Thirty-seven percent of women attended two of the screening programmes and seventeen percent attended one screening programme. Ten percent participated in none of the programmes.
One way to increase participation in cancer screening is through reminders such as personalized phone calls, letters and text messages. 7,11,12 A further way of encouraging screening uptake could be advice to take part in one type of cancer screening when attending another. In this way, attendance at cancer screening could act as a 'teachable moment' for behaviour change, affirming the current choice to attend the screening to motivate engagement with other screening programmes. Teachable moments represent a time in which people are more likely to examine how their habits can impact their physical health. 13 They have revealed favourable results, including increased knowledge and safer behaviours. 14 However, it is not known whether women would be willing to receive advice about screening and early detection of other cancers when attending for cancer screening and whether they would find that acceptable. Yet this is key: For an intervention to be as successful and effective as possible, it is necessary to ensure acceptability to both the people who deliver the intervention and those who receive it. 15,16 Recent developments in the study of acceptability have advocated that acceptability is a multi-faceted construct reflecting anticipated or experienced cognitive and emotional responses to an intervention.
The Theoretical Framework of Acceptability (TFA) 15 There is some existing research on willingness to receive lifestyle advice within screening programmes. The results revealed that the majority of participants expressed willingness to receive lifestyle advice at cervical, breast, lung and bowel cancer screenings. However, a smaller number indicated that they would be less likely to take part in lung cancer screening if lifestyle advice was provided. 17,18 More detailed information on acceptability is needed and views on advice about screening and early detection of other cancers have not been investigated. Just as barriers and uptake differ between screening programmes, 19 acceptability may also differ with regard to different types of advice.
This study focuses on breast cancer screening as a teachable moment to encourage screening and early detection of other cancers.
We aimed to investigate and compare women's willingness to receive advice about cervical cancer screening participation, bowel cancer screening participation and advice on cancer symptom awareness when attending breast cancer screening and women's prospective acceptability of receiving such advice. A secondary objective was to develop a measure of acceptability underpinned by the TFA, to support these investigations.

| Study design
The study involved a cross-sectional online survey of women eligible for all three national screening programmes.

| Participants
Women fulfilled the inclusion criteria if they were aged between 60 and 64 years, lived in the United Kingdom and had previously taken part in the UK national breast cancer screening programme.  Microsoft Forms, women were presented with an online information sheet explaining the purpose of the study and were asked to complete a consent form before starting the questionnaire (see below and File S1) if they wished to take part and fulfilled the inclusion criteria.

| Sociodemographics variables
Participants were asked to confirm their age, educational attainment, marital status, ethnicity and postcode. Postcode was subsequently converted into indices of multiple deprivation deciles, 20 with 1 representing the most deprived decile and 10 the least deprived decile.

| Health and health-related behaviours
Participants were asked to report their recent daily fruit and vegetable consumption, weekly physical activity, smoking status and history of cancer. For analyses, those who consumed five or more portions per day were compared to those who ate fewer fruit and vegetables.

| Screening history
Participants were asked to report the timing of their last mammography, cervical screening attendance and participation in bowel cancer screening (either home testing kits or bowel scope screening).

| Prospective acceptability
Acceptability of receiving advice on cervical screening, bowel screening and cancer symptoms was measured using two subscales reflecting cognitive acceptability and affective acceptability. Every item was asked in relation to each type of advice. This was a newly developed measure for this study. Items were developed to capture the domains of the TFA 16

| Analyses
Two quality assurance measures for online surveys were used before data analysis. First, 'speeders', participants who completed the online survey in less than a quarter of the average survey time, were excluded from analyses. Second, participants who did not respond correctly to a direct question ('To make sure you're reading the questions carefully, we'd like you to select the "Agree" response to this item') were also excluded.
Using previous estimates of willingness to receive lifestyle advice at breast cancer screening, 17 Table 1 reports the sample characteristics. The majority of participants were married (n = 208, 65%), of White ethnicity (n = 309, 96%) and educated to below bachelor's degree level (n = 196, 61%). A substantial proportion were current or ex-smokers (n = 129, 40%). The majority of women did not meet the recommended guidelines for fruit/vegetable consumption (n = 215, 67%).
A total of 24% (n = 78) participants indicated that they did no physical exercise at all. The majority of participants were up to date with breast cancer screening (n = 271, 84%); somewhat fewer were up to date with cervical screening (n = 217, 67%) and bowel screening (n = 254, 79%).

| Willingness to receive advice and prospective acceptability of receiving advice
Over 85% of women indicated that they would be willing to receive information about cervical cancer screening, bowel cancer screening and early symptoms of other cancers at a breast cancer screening appointment (see Table 2). Cochran's Q indicated that willingness to receive advice at a breast cancer screening appointment differed according to the content of that advice (Q = 15.2, p< .001). While the proportion of women willing to receive advice about bowel cancer screening (90%) and early symptoms of cancer (92%) was similar, willingness to receive advice about cervical cancer screening was significantly lower (86%, McNemar χ 2 = 11.12, p< .01).
The preferred ways to receive advice were by leaflet (preferred by 41% of women) and discussion with the mammographer (preferred by 30% of women) and before the appointment (preferred by 27% of women), at the appointment (preferred by 44% of women) or with results (preferred by 22% of women; see Figures 1 and 2).
Cognitive and affective acceptability were high for all three forms of advice (see File S3). The Wilcoxon signed ranks test indicated that cognitive acceptability of receiving advice about early symptoms of cancer was higher than that for receiving advice about bowel cancer screening (z = −6.89, p< .001), which in turn was higher than that for receiving advice about cervical cancer screening (z = −5.12, p< .001). Affective acceptability was similar across the three types of advice.

| Factors associated with willingness to receive advice
Univariate logistic regression (see Table 3 Women would prefer such advice to be provided through a leaflet or discussion with the mammographer at the breast cancer screening appointment although some would prefer the information to be provided before the appointment or with their breast screening results. Existing interventions that have utilized the breast cancer screening programme as a teachable moment have focused on early detection of breast cancer by raising awareness and encouraging early presentation of symptoms 21 or prevention. 22 The current study extends this by considering the early detection of different cancers.
The high levels of willingness and acceptability are promising and comparable to previous findings that have looked into willingness to receive lifestyle advice as part of screening programmes. 17,18 However, there remains a proportion of women who would not be willing to receive advice and, more concerningly, approximately 13% may be reluctant to attend their breast screening appointment if they knew that advice about screening and early detection of other cancers would be provided. This concurs with the findings about the potential to give lifestyle advice as part of the breast or cervical screening programmes where a minority of people reported that provision of advice would make them less willing to participate in future cancer screening. 17 Any benefits of such an intervention in terms of uptake of other screening or prompt help-seeking would thus need to be carefully weighed up against the potential risk of reduced breast screening uptake.
The new measures of cognitive and affective acceptability underpinned by the TFA 16 were successful in determining similarities and differences in acceptability between different types of advice and the measure showed construct validity in the associations with willingness to receive advice. There is scope to test the measures further to determine predictive validity and whether statistically significant differences in affective or cognitive acceptability translate into meaningful real-world differences. Prospective acceptability was a key factor associated with willingness to receive advice, offering further support for the TFA and reinforcing the importance of ensuring that interventions are acceptable to the target group.
Further work could focus on the practitioner's views of acceptability and feasibility, or adapt the measures to assess concurrent and retrospective cognitive and affective acceptability of patients.    23 whereas a key concern for bowel screening is embarrassment over providing a stool sample. 19,24 Cervical cancer screening is more invasive, and there are also specific barriers to cervical cancer screening in this age group such as increased discomfort and low perceived risk. 25
---- However, this study has limitations: The study used a selfreported questionnaire in a cross-sectional design; therefore, causation cannot be established. Women were not asked about hysterectomy: A proportion of respondents may have been ineligible for cervical screening, which in turn may have affected recent screening attendance and willingness to receive advice about cervical cancer screening. The data were also collected in June 2020 when the national breast cancer screening programme had been paused in the United Kingdom due to the COVID-19 pandemic. It is unknown how this may have affected the data. Despite this, relationships could be deduced, and the sample size provided power to detect associations.

Yes
A further limitation is that the sample included very few women from ethnic backgrounds other than White. It is therefore not possible to generalize the findings to the wider population, especially as women from ethnic minority backgrounds tend to show lower screening uptake. 28 Finally, surveys often find that self-reported screening uptake is higher than uptake reported in national data, likely due to response bias and indeed that was the case in this study. However, as previous participation in breast screening was an inclusion criterion for the study, bowel screening participation would be expected to be higher in our sample than the general population, given that women who have taken part in breast screening are more likely to participate in the other screening programmes. 30

| CONCLUSION
On the one hand, there is high willingness and high acceptability towards using breast cancer screening as a teachable moment.
However, the few women who find it unacceptable and are less willing to receive the advice about screening and early diagnosis may be the intended target of such an intervention and the very women who would benefit the most.