Barriers and facilitators to colonoscopy following fecal immunochemical test screening for colorectal cancer: A key informant interview study

Highlights • A range of practical, psychological & social barriers to colonoscopy were reported.• Psychological barriers (e.g., fear of pain) were considered to be the most pertinent.• Several new barriers, including fear of getting and spreading COVID were described.• The results advocate a multifaceted approach to reducing barriers to colonoscopy.• Providing information on the risk of COVID might increase uptake during lockdowns.


Introduction
Colorectal cancer (CRC, also referred to as 'bowel cancer') is a leading cause of morbidity and mortality in Europe [1]. Several large randomized controlled trials (RCTs) have shown that regular fecal immunochemical test (FIT) screening, between the ages of 45 and 80, can significantly reduce the mortality of the disease among people who complete the test [2]. As a result, many European countries have implemented FIT-based screening programs for the early detection of CRC [3].
As with all screening, the extent to which the benefits of FIT screening are realized is highly dependent on the uptake of the screening test, as well as any necessary follow-up investigations (colonoscopy being the gold standard) [3]. In a recent international survey of 35 FIT screening programs, however, Selby et al. found that the mean proportion of participants with a positive FIT result who complete follow-up colonoscopy was only 79%, with completion rates ranging from 39% in the program with the lowest level of follow-up, to 100% in the country with the highest [4].
Non-attendance at colonoscopy is a major source of inefficiency within CRC screening programs and is associated with a range of https://doi.org/10.1016/j.pec.2021.09.022 0738-3991/© 2021 The Author(s). Published by Elsevier B.V. CC_BY_4.0 adverse outcomes, including increased risk of CRC, advanced stage diagnosis and CRC death [5]. As a result, there is much current interest in understanding the reasons for lack of follow-up, and how to prevent it [6,7].
With regards to the quantitative literature, a number of studies utilizing surveys and electronic health records have been conducted, demonstrating evidence of disparities in uptake by socioeconomic position and ethnicity [6]. While such studies are useful in terms of identifying low uptake groups, they tend to focus more on demographic, clinician, and program factors, and less on the important reasons why patients decline the test offer [6]. To this end, a wide range of qualitative studies have been performed.
To date, the majority of qualitative research examining nonattendance at colonoscopy has focussed on barriers to colonoscopy as a primary screening test for asymptomatic adults, as opposed to a diagnostic test for those with an abnormal screening result [7]. Indeed, a recent review of the literature found that, of 57 qualitative studies exploring barriers and facilitators of colonoscopy use, 54 focussed on 'screening colonoscopy' (only two focussed on 'follow-up colonoscopy'), nearly all of which (n = 48) were conducted in the USA, where the delivery of screening is opportunistic, and highly different from the organized programs offered in Europe and the rest of North America [7]. Other reviews of barriers to endoscopic examinations have drawn similar conclusions. For example, in a separate review of barriers to colonoscopy, Lim et al. included studies that explored the perspectives of healthcare professionals, but were unable to find any conducted outside of North America [8]. One review (Travis et al. 9) of the barriers to flexible sigmoidoscopy screening did find several studies conducted within Europe; however, given the differences between the two tests (prep time, insertion depth, sedation options, etc.), and their indications (screening vs. follow-up), the findings are not generalizable to colonoscopy [9].
Further qualitative studies with patients and healthcare professionals are needed to better understand the barriers to colonoscopy as a follow-up test. The aim of this study, therefore, was to develop an understanding of non-attendance at follow-up colonoscopy in the context of an organized FIT-based CRC screening program, by interviewing the healthcare professionals involved in the decisionmaking process.

Participants
As little is currently known about non-attendance at follow-up colonoscopy within organized FIT-based CRC screening programs, and follow-up of a positive result is a nurse-led process in the English Program, we decided to conduct key informant interviews with 'Specialist screening practitioners' ('SSPs'): specialist nurses, employed by the English Bowel Cancer Screening Program (BCSP), who specialize in assessing patients' health for follow-up colonoscopy, and provide support in deciding whether to undergo further examination (they typically assess about six patients a week -See Fig. 1 for an overview of the patient pathway and the SSPs role within it).

Recruitment
Participants were recruited through the SSP Knowledge Hub (using convenience sampling): an online forum accessed by approximately one third of SSPs working in England. SSPs with access to the knowledge hub were sent a participant information sheet, which outlined the purpose of the study and directed interested individuals to contact the principal investigator (RK) via email. The interviewer had no prior relationship with the participants.

Setting
All interviews were conducted online, between October and November 2020, using one of three virtual platforms, namely: 'Microsoft Teams', 'Zoom' and 'NHS Attend Anywhere'.

Data collection
Interviews were conducted by Dr Robert Kerrison (PhD): a male Senior Research Fellow with nine years' experience in the field of Behavioral Science and Cancer. In the first instance, 15 interviews were performed. Additional interviews were then carried out in sets of 3, until no new themes were found in the data. Interviews lasted up to 75 minutes and were conducted using a semi-structured interview guide, which was pilot tested with one SSP prior to data collection. Questions focussed on SSPs experiences dealing with FIT results, the pre-colonoscopy assessment and the colonoscopy referral (see Appendix 1). An audio recorder was used to audio record the interviews (field notes were also taken during the interviews). The recordings were anonymized, transcribed verbatim (RK), and deleted immediately after.

Data analysis
Two authors (RK and ET) coded a proportion (n = 4, 19%) of the transcripts, using a coding framework synthesized from the existing literature (see Appendix 2) [7]. Thematic analysis was simultaneously applied to identify new barriers and facilitators not previously described. A revised framework was subsequently developed, which led to the removal of redundant codes (i.e. codes that did not appear in the transcripts), the addition of new codes (i.e. codes that were not previously described in the coding framework) and the revision of existing codes (some codes were relabeled to better reflect the data). One author (RK) coded the remaining transcripts (n = 17, 81%) using the revised framework. Several further codes were subsequently added to the framework as new transcripts were analyzed (previously coded transcripts were then revisited to check for the presence of newly identified codes). Superordinate themes, themes and subthemes were then developed by three authors (RK + ET + CD) through an iterative process of comparing, reexamining, and grouping the codes until consensus was achieved. The superordinate themes, themes and subthemes were shared with, and considered by all authors to ensure they were consistent and apposite. The data were coded and analyzed in Excel. The number of interviews in which subthemes were identified was also reported, to help assess the extent to which they might be important. To minimize participation burden, participants were not invited to review the findings.

Rigor
After each stage of data analysis, two reviewers (RK and ET), plus a third reviewer (CD), discussed the thematic findings and resolved disagreements to help maintain theoretical validity (i.e., reliability of data interpretation) [10].

Transparency
The reporting of this interview study follows the Consolidated Criteria for Reporting Qualitative Research (COREQ) guidelines (Appendix 3) [11]. A database of the coded text is available from Open Science Framework provided for further transparency (see: https://osf.io/5fe2c/).

Ethics
The study was approved by University College London's Joint Research Office (reference: 599/002) on the 6th of July 2020.

Participant characteristics
In total, 21 SSPs participated in the study. The majority were female (n = 20, 95.2%). The mean number of years worked as an SSP was 6.6 (range: 2-13 years; Table 1). None of the participants dropped out or withdrew from the study.

Revisions to the framework
A number of revisions to the original framework were made during the analysis process, with 39 subthemes added, 16 removed and 10 relabeled (an overview of the revisions made to the framework is provided in Table 2).

Description of themes
In total, five main types of barriers and facilitators were identified: Sociocultural, Practical, Psychological, Health-related and COVID-related. Psychological and sociocultural factors centered on intrinsic constructs, such as cultural taboos, concerns about the procedure, and knowledge about CRC. Conversely, practical, healthrelated and COVID-related factors centered on more extrinsic constructs, such as indirect costs associated with attending the precolonoscopy assessment or colonoscopy appointment, existing health conditions, and shielding. Fig. 2 provides a diagrammatic overview of the barriers and facilitators of colonoscopy use. The following provides a detailed description of the barriers and facilitators identified; illustrative quotes and the number of SSPs who discussed each of the barriers and facilitators are presented in Table 3.  only about follow-up colonoscopy, but also in relation to their decision about attending the pre-colonoscopy assessment, for which they often rely on friends and family for transport to the clinic, or as emotional support. In some instances, family members were reported to go beyond the provision of practical and emotional support, and actively influenced the individual's decision making, with Family influenced participation reported by a number of SSPs. For some patients, the primary care provider was said to play an important role in the decision to attend colonoscopy, specifically with regards to receiving a GP Recommendation. SSPs also reported that hearing stories in the media, or from other people, has a significant effect on patients' willingness to attend colonoscopy. SSPs frequently made reference to Media Coverage of celebrity stories as having a positive influence; conversely, Hearing other people's experiences with colonoscopy was described as a barrier to follow-up colonoscopy, with (negative) experiences of family and friends often deterring individuals from having the test.
Knowing someone with CRC was also described as an important motivating factor, particularly where the person affected is a close friend or family member.

Cultural and religious beliefs and attitudes.
SSPs described a range of cultural barriers to colonoscopy. Foremost among these was the fact that Colonoscopy, colon and rectum are 'culturally taboo',    (21) """If they're very anxious, and they, they can't take it in, there's somebody else there to actually take that in, and also, having somebody there as well will often help to resolve transport issues as well, because they'll say, "Oh, no, I'll take you" or "we know 'so and so' will take you" (Participant 12) 1.1.2. Family influenced participation (10) "I find the men who have the wives, the wives will say "he's having it, and that's it", you know, they've not choice." (Participant 1) 1.1.3. Media coverage (9) "We do see an upsurge when celebrities say that they '  Fatalistic beliefs were a less frequently reported cultural barrier to colonoscopy, but one which was considered particularly salient to the White Gypsy / Irish Traveler community. SSPs also reported that men are generally more reluctant to engage with colonoscopy, but that this cultural phenomenon was not exclusive to colonoscopy, but other forms of healthcare as well (Gender and engagement with healthcare).
In addition to cultural barriers to colonoscopy use, SSPs described several religious barriers. Foremost among these was being Unable to have a male endoscopist, which was a barrier that was specifically reported by Muslim women, who did not want to be seen or touched by a male other than their husbands, meaning that they requested that only female staff, including interpreters, be present during the procedure, and sometimes the pre-colonoscopy assessment as well. Jehovah's Witnesses were reported to face the additional barrier to colonoscopy of being Unable to accept blood products, which meant that some would choose not to undergo the colonoscopy in case this was required.

Practical factors 3.3.2.1. Language barriers.
Language was described to be a key barrier for patients whose first language was not English and was also reported as a barrier for patients who had hearing difficulties or previously experienced a stroke. This barrier manifested itself in a number of ways, from patients missing the pre-colonoscopy appointment as the family / friend who usually interprets their mail for them was away at the time of invitation, to SSPs being unable to conduct the pre-colonoscopy assessment as no interpreter had been organized (some centers require an NHS interpreter to be translate the assessment if the patient does not speak English).

Competing priorities and accessibility issues.
SSPs discussed how competing priorities, such as Family, work and religious commitments, could act as barriers to colonoscopy. Ramadan was reported to be a difficult time for Muslims to attend colonoscopy, as the required fasting makes it difficult to complete bowel preparation. Some participants also miss the pre-colonoscopy clinic as they are Traveling / on holiday at the time, although SSPs reported that these patients usually rebook.
The location of the hospital/clinic was reported to be a barrier to colonoscopy for a number of reasons. Transport/travel was often a barrier to attendance because of the time and/or distance patients have to travel to attend, along with the Indirect costs associated with traveling, and the problem of a Lack of car parking and the expense of on-site parking facilities.
SSPs also reported that patients sometimes did not attend the initial pre-colonoscopy appointment because the Initial invitation was not received; however, these individuals usually received the second invite, and attended that appointment, so this only incurred a short delay (see Fig. 1 for an overview of the invitation pathway).

Unexpected events on the day of the appointment.
SSPs reported a range of events that can occur on the day of the appointment and sometimes act as barriers to colonoscopy. Such events include Feeling unwell, Personal emergency and Failed bowel preparation. With the exception of failed preparation, all were sufficient to prevent the individual from attending their colonoscopy appointment, although SSPs indicated that most would call and rebook. For those individuals with failed preparation, however, it was not until they got to the hospital and attended their appointment that it became apparent the bowel prep had failed. In most of these cases, SSPs reported the bowel prep failed because the patient had only partially followed the instructions Fig. 2.

Psychological factors 3.3.3.1.
Concerns about the procedure. SSPs reported a wide range of patient concerns about the procedure during the pre-colonoscopy assessment, some of which related to experiential aspects of the procedure, while others related to possible treatments and outcomes. Among the most frequently reported were Concerns about the bowel preparation, including concerns about incontinence on the journey to the hospital, having to fast in order to do the bowel preparation, and the volume and taste of bowel preparation. The bowel preparation was said to be a particular concern for people who had previously had a colonoscopy. Indeed, SSPs commented that those patients often found the bowel prep to be worse than the colonoscopy itself.
Fear of pain and discomfort was another prominent barrier to colonoscopy use. When asked whether there were any questions patients frequently ask during the assessment, SSPs first response consistently was that patients ask if it will be painful. Concerns about the availability and necessity of sedation were also common, with patients wanting to know whether they can be 'knocked out' during the procedure, and in some instances, were worried that they might not wake up again.
Concerns about test invasiveness were frequently cited as a key barrier to colonoscopy, with concerned patients often requesting a scan instead. Concerns about perforation and procedural risks were also reported. When discussing the risks of the procedure, SSPs reported that patients often presented Concerns about the practitioner performing the test, stressing that they 'did not want anyone practicing on them'.
Shame and embarrassment were commonly reported by SSPs as being patient barriers to follow-up colonoscopy, with patients being embarrassed about 'having an accident' or 'being exposed', during the colonoscopy, as well as having to discuss 'bowels and bowel habits', during the assessment.  (13) "They're more worried about COVID than getting a cancer" (Participant 7) 5.1.2. Unable to leave the house due to shielding (2) "There were a few that said that they were shielding and they didn't want to come because they were shielding" (Participant 9) 5.1.3. Fear of spreading COVID (1) "They're too afraid to expose to the hospital, because one of their family members maybe is very ill" (Participant 7) 5.2. Impact of COVID measures 5.2.1. Unable to get in contact with patients (4) "A lot of them, because our number comes up 'private number', they won't answer" (Participant 1)

Patients unable to bring friend / family for emotional support (3)
"Um, what else we do let patients to bring a relative, although with COVID, we don't allow relatives anymore" (Participant 5) 5.2.3. Patient and household required to self-isolate prior to procedure (2) "Um, I have had a patient more recently, um, who was due to have a colonoscopy, but they broke the isolation rules at that point for the place where they were having the colonoscopy, so we had to cancel it" (Participant 20)

Knowledge about CRC, screening and colonoscopy. Several
SSPs reported that patients often state that they do not feel as though they need colonoscopy, as they 'don't have any symptoms' and 'can't see any blood when checking their stool' (Lack of understanding that bowel cancer can be asymptomatic and the test is looking for invisible traces of blood). SSPs also reported that a lack of knowledge about the procedure often proved problematic, with patients having no concept when being told that a camera would be used to visualize the large bowel (Lack of awareness and understanding of colonoscopy procedure).

3.3.3.3.
Emotional responses during the assessment. SSPs reported that patients exhibited a wide range of emotions during the assessment, several of which acted as barriers to follow-up colonoscopy. Anxiety was commonly reported by SSPs, who discussed how the overwhelming majority of patients are anxious, with many believing that they have cancer.
Another emotional response that SSPs frequently reported patients exhibiting was Denial, as a number of patients do not believe the result of their screening test, often providing alternative explanations as to why it was positive (e.g., hemorrhoids). In those instances, SSPs reported that patients did not want to proceed with colonoscopy, and sometimes wanted to repeat the screening test instead. SSPs also reported that a number of patients experienced Shock, as they said patients often completed the screening test expecting the result to be negative, and so were not prepared for a positive result. Avoidance was also reported as an emotional barrier to colonoscopy, with SSPs highlighting how some patients 'would rather not know' and 'simply did not want to have colonoscopy'.
In all instances, SSPs reported 'having to work hard' to reassure patients and help them overcome their emotions, in order to deliver an effective assessment.

3.3.3.4.
Cognitive abilities and ability to make an informed decision. SSPs described several cognitive abilities that were required to make an informed decision to undergo colonoscopy. Lack of capacity (for instance, in relation to dementia, Alzheimer's, or patients with learning difficulties), Low Health Literacy and Memory issues were all said to present SSPs with significant challenges in proceeding with colonoscopy. With regards to lack of capacity and memory issues, SSPs said it was often necessary to hold a 'best interest' meeting, where the individual carer, along with a panel of experts, including an SSP, would make a decision on behalf of the patient. Health literacy issues were different in that patients could make a decision for themselves, but often needed the information presented to them differently (e.g., via 'easy read' materials).

Perceived
CRC risk and perceived benefits of colonoscopy. Elevated risk perception was a key motivating factor for many patients, with these patients more likely to book and attend colonoscopy. Several SSPs indicated that Having a family history of CRC or Having CRC symptoms were frequently stated as reasons for accepting and attending colonoscopy. Perceived benefits of having the colonoscopy procedure were also reported to be key motivating factors for accepting and attending the colonoscopy procedure. SSPs indicated some patients feel that the test will bring Peace of mind and for others fed into their behaviors to maintain good health through their Proactive desire to stay healthy.

Health-related factors 3.3.4.1. Existing health conditions and medical history affecting clinical eligibility to have the test.
SSPs explained that some patients are Clinically ineligible or inappropriate, either because they have an existing health condition, or they are on certain medication, such as blood thinners. In these instances, SSPs described having to discuss how best to proceed with a consultant. Responses varied, with some patients being recommended no follow-up, and others CT colonography.

Existing health conditions and medical history affecting patient willingness to have the test.
Even among patients who are clinically eligible, existing health conditions and the individual's medical history were still reported to play an important role in a patient's decision to proceed to colonoscopy. SSPs discussed how, for some patients, Existing health conditions as a competing priority prevented progression to colonoscopy, whereas the perceived impact of an Existing health condition interfering with ability to do the bowel preparation served as a significant barrier for others.
Finally, patients who had previous colonoscopies often declined follow-up colonoscopy through the BCSP, either because they felt it was unnecessary because they'd had a Recent colonoscopy, or because they'd had negative Previous personal experiences with colonoscopy or other medical investigations.
3.3.5. COVID-related factors 3.3.5.1. Impact of COVID. SSPs reported several COVID-related barriers to colonoscopy, including being Unable to leave the house due to shielding and Fear of getting COVID. In some instances, the 'fear of getting COVID' was reported to be greater than the fear of a possible colorectal cancer diagnosis. COVID-related fear sometimes extended beyond the individual patient, to include Fear of spreading COVID, whereby individual's (and their households) were concerned about spreading COVID to their family and friends, (in some cases there was pressure from family and friends for them not to attend).

Impact of COVID measures.
In addition to COVID itself presenting barriers to colonoscopy, the measures implemented to mitigate the risk of COVID were also reported to present barriers to colonoscopy. For example, several centers reported that delivering pre-colonoscopy assessments over the phone (i.e. to reduce the risk of COVID) led to a lower uptake, primarily because the caller ID shows the SSPs as calling from a private number, from which many people were thought to be reluctant to take calls (SSPs reported they had more success when they called from a non-hospital phone). Having to self-isolate prior to the colonoscopy also led to issues, with patients' appointments frequently needing to be rescheduled, as individuals, or members of their household, had not shielded during the required period.

Main findings
This study identified five main types of barriers and facilitators of colonoscopy use: sociocultural, psychological, practical, health-related and COVID-related. Of these, Psychological factors appeared to be the most important barriers. Specifically, 'concerns about the procedure' were identified the most frequently ('concerns about doing the bowel preparation' and 'fear about pain and discomfort' in particular), followed by emotional responses during the assessment (e.g., 'Anxiety' and 'Denial') and 'Cognitive abilities and ability to make an informed decision' (e.g., 'Capacity'). Psychological factors also appeared to be the most important facilitators of colonoscopy use, with 'perceived risk and perceived mortality' being the most frequently discussed.
Importantly, this study identified barriers and facilitators that were specific to colonoscopy among people who receive a positive FIT result. Some of the identified barriers were applicable to a broad range of patients, such as 'lack of support from friends and family' and 'emotional states', while others, such as those relating to modesty and the role of male staff in Muslim women's decisionmaking, were specific to certain patient groups.

Comparison with existing literature
The results of this study add to the findings of our previous review [7] in several ways. First, by capitalizing on the experience of SSPs, the present study identifies unique barriers for specific patient groups, not previously interviewed, including Jehovah's Witnesses and Muslims (e.g., being unable to accept blood products). Second, it identifies unique contextual issues, not pertinent to screening colonoscopy, such as emotional reactions to receiving an abnormal FIT result (e.g., Shock that the test result was positive, Denial that the test result was accurate). Third, it identifies cultural barriers, within the UK, relating to gender and engagement with healthcare (with men living in the UK being less likely to engage in healthcare than their female counterparts) [12].
This review also identifies a number of COVD-related barriers to colonoscopy, including 'fear of getting COVID at the hospital' and 'fear of spreading COVID to others'. The findings are consistent with Rees et als'. hypothesis, that: "Anxiety about COVID-19, family pressures, logistical considerations, such as carer responsibilities, and travel to and from the hospital while adhering to social distancing, might also be barriers" [13]. Providing patients with information regarding the risk of contracting COVID (~1 in 200) might reassure patients about the risks of getting and spreading COVID [14,15], thereby facilitating uptake during possible future lockdowns. Further research is needed to test this hypothesis.
Finally, it is important to note that, while this study identified several unique barriers to follow-up colonoscopy (e.g., 'Denial about the FIT result', 'Lack of understanding that bowel cancer can be an asymptomatic disease and the test is looking for invisible traces of blood', etc.), it also identified a number of barriers common to primary colonoscopy and sigmoidoscopy screening. For example, in a recent review of the literature, Lim et al. found that a lack of 'Social support', 'Knowledge' and 'Perceived risk' were all barriers to primary colonoscopy use [8]. Similarly, Travis et al. found 'shame and embarrassment', 'procedural pain and discomfort' and 'competing priorities' all inhibited primary sigmoidoscopy use in a review of the barriers to sigmoidoscopy screening [9]. Given the similarities between primary endoscopy and follow-up, it's possible that some interventions, designed to address barriers for one indication, could address barriers for another. Consideration should be given to this hypothesis when testing interventions to promote colonoscopy use.

Implications for future research
This study has several additional implications for future research. First, further qualitative research with patients and members of the public is needed to verify the results of this study and to explore the issues from the perspectives of service users. Second, quantitative research is needed to understand how barriers and facilitators interact with one another, and which of the perceived barriers and facilitators are significantly associated with non-attendance at colonoscopy. Third, randomized controlled trials of complex interventions, which target a range of practical, psychological and sociocultural barriers are required to identify effective strategies to reduce barriers and improve colonoscopy attendance. Adopting a theoretical framework would be particularly useful in relation to this last item. For example, the Theoretical Domains Framework allows researchers to map psychological targets onto a framework that, in turn, could be used to identify behavior change techniques that are potentially effective at modifying those targets [16]. Previous research based on this approach has been effective at changing a range of behaviors, and is proposed to offer the best approach to changing health behaviors [16][17][18].

Limitations
This study has several limitations. Most importantly, it was conducted with SSPs, as opposed to patients. As such, the findings may not reflect the full range of barriers and facilitators perceived by patients, only those patients choose to disclose to SSPs. Furthermore, SSPs were recruited from the SSP Knowledge Hub. As such, the possibility of there being some selection bias cannot be dismissed. Finally, SSPs from only a proportion of screening centers participated in the study. As such, the findings may not reflect additional barriers and facilitators specific to external contexts and patient groups.

Strengths
This study also has a number of strengths. Most importantly, following each stage of data analysis, two reviewers (RK and ET), plus a third reviewer (CD), discussed the thematic findings and resolved disagreements through discussion to help maintain theoretical validity (reliability of data interpretation) [19]. Moreover, we used framework analysis to inform our interpretation of the data. This method of analysis is not aligned with a particular epistemological, philosophical, or theoretical approach, and can be adapted for use with many qualitative approaches that aim to generate themes without bias [20]. Finally, pragmatic validity (efficacy and transferability of findings) was improved by inclusion of participant characteristic tables, providing context around the individuals, allowing readers to judge the usefulness of the findings [21].

Conclusion
The results imply that a range of barriers to follow-up colonoscopy exist, with psychological barriers being the most pertinent among these. Future studies, conducted with patients and members of the public, are needed to explore the barriers to colonoscopy further.

Practice implications
Complex interventions, which address a range of psychological, practical and sociocultural barriers to follow-up colonoscopy are required to reduce non-attendance and improve service delivery.