Health literacy skills for informed decision making in colorectal cancer screening: Perceptions of screening invitees and experts

Abstract Background The process of informed decision making (IDM) requires an adequate level of health literacy. To ensure that all individuals have equal opportunity to make an informed decision in colorectal cancer (CRC) screening, it is essential to gain more insight into which health literacy skills are needed for IDM. Our aims were (i) to explore how individuals make a decision about CRC screening and (ii) to explore which skills are needed for IDM in CRC screening and (iii) to integrate these findings within a conceptual framework. Methods We conducted 3 focus groups with individuals eligible for CRC screening (n = 22) and 2 focus groups with experts in the field of health literacy, oncology and decision making, including scientific researchers and health‐care professionals (n = 17). We used framework analysis to analyse our data. Results We identified and specified ten health literacy skills, which varied from the ability to read and understand CRC screening information to the ability to weigh up pros and cons of screening for personal relevance. The skills were linked to 8 decision‐making stages in CRC screening within a conceptual framework. We found differences in perceptions between screening invitees and experts, especially in the perceived importance of CRC screening information for IDM. Conclusions This study provides insight into the decision‐making stages and health literacy skills that are essential for IDM in CRC screening. The proposed conceptual framework can be used to inform the development of context‐based measurement of health literacy and interventions to support IDM in cancer screening.

Informed decision making has been described by Timmermans as a process that includes 4 decision-making stages: (i) becoming aware of the decision to be made, (ii) structuring decision options and outcomes, (iii) evaluating decision options for personal relevance and (iv) making the final decision. 3 An informed decision is considered to be the outcome of these stages and is commonly defined as one that is "based on relevant knowledge, consistent with the decision-maker's values and behaviourally implemented." 4,5 Accordingly, screening invitees are explicitly required to deliberate harms and benefits to make an informed decision about participation in CRC screening. As IDM relies on the application of information to one's own situation, it is assumed that this decision-making process requires an adequate level of health literacy. 6 Health literacy has been described by Sørensen et al 7 as 4 aspects of information processing (access, understand, appraise and apply).
Access refers to the ability to seek, find and obtain health information.
Understand refers to the ability to comprehend the health information that has been accessed. Appraise refers to the ability to interpret, filter, judge and evaluate the health information that has been accessed.
Apply refers to the ability to communicate and use the information to make a decision to maintain and improve health. Health literacy is dependent on health-care content and context. For instance, the decision-making process for CRC screening, in which individuals need to understand the disease characteristics of CRC and weigh up the pros and cons of screening, requires different health literacy skills than diabetes self-management, in which individuals have to adhere to medication regimes and maintain a healthy lifestyle. 8 The conceptualization of health literacy skills has implications for its measurement and consequently, for intervention development. 9 Decision making about CRC screening is complex and it remains an ongoing challenge to inform all screening invitees in an accessible and understandable way. 10 To ensure that all individuals have equal opportunity to make an informed decision in CRC screening, it is important to understand which health literacy skills are perceived as essential for IDM in this particular context. This knowledge is necessary for the development of context-specific health literacy measures and tailored interventions that support IDM in screening. While informed decisions seem to be a central outcome in the conceptualization of health literacy, few studies have explored the integration of models of IDM and health literacy. 6,7 In addition, there is a paucity of research on what exactly constitutes an informed decision in cancer screening from the perspective of screening invitees. The aims of this study were therefore (i) to explore how individuals eligible for screening make a decision about screening and (ii) to gain more insight into which health literacy skills are needed for IDM about CRC screening and (iii) to integrate these findings within a conceptual framework.

| Study design
We conducted 2 focus groups with experts representing different fields of expertise (health literacy, oncology and decision making) including scientific researchers and health-care professionals (n = 17) and 3 focus groups with individuals eligible for CRC screening (n = 22).
The focus group interviews were moderated by MF from May to October 2015 in the Netherlands, where a nationwide CRC screening programme is being implemented since 2014 (see Box 1). An advantage of focus groups is their use of group dynamics to stimulate the discussion, 11 which provided us with deeper insights into individuals' considerations about CRC screening participation. According to Dutch law, this study was waived from requiring medical ethical approval.
Nonetheless, we guaranteed the anonymity of the participants and ensured that informed consent was obtained from all participants prior to conducting the focus group interviews.

| Focus group interviews with experts
The experts (scientific researchers and other professionals) were recruited from the working group "Shared Decision Making" at the Academic Medical Centre in Amsterdam, the Netherlands (n = 8), and the working group "Scientific research" of the Dutch Health Literacy Alliance (n = 9; Table 1). The Dutch Health Literacy Alliance was es-

Box 1 Background information on Dutch CRC screening programme
In the Netherlands, a nationwide colorectal cancer (CRC) screening programme has been implemented since 2014. By 2019, all individuals between the ages 55-75 years will be invited every 2 years to perform an immunochemical faecal immunochemical test (FIT) at home. The CRC screening invitation includes an announcement letter (which is sent 2 weeks prior to the invitation), a leaflet about CRC and CRC screening, a leaflet including instructions about performing the FIT, the FIT and an answer form. Additional information about CRC screening is available on the website of the National Institute for Public Health and the Environment. 1 When the FIT is positive (ie blood is found in the stool sample), individuals are invited for further diagnostic follow-up: a colonoscopy.
(iii) whether other stages of decision making should be considered for IDM about CRC screening participation.

| Focus group interviews with the target group
Five hundred individuals (aged 55-75 years) were recruited from general practices in the southeast of Amsterdam. They were randomly selected and invited by postal mail. One hundred and forty of them expressed interest to participate in research on CRC screening (by means of a prepaid response card). Of these 140 individuals, 46 were contacted for another study on knowledge of CRC screening. 10 Of the remaining 94 individuals, we were able to contact 41 of them by phone.
We were unable to reach the other 53 individuals in the previous study or current study. Twenty-two individuals finally participated in the 3 focus group interviews (Table 1). The total number of included participants was based on data saturation. Two focus groups were conducted at the Academic Medical Centre in Amsterdam, and 1 focus group was conducted in a general practice in the southeast of Amsterdam.
The specific aims of the focus groups were as follows: (i) to examine which decision-making stages and health literacy skills are being used in decision making about CRC screening and (ii) to examine which stages and skills were perceived as being essential to make an informed decision about CRC screening participation. During the focus group interviews, participants were given the opportunity to ask questions about the CRC screening information. To gain insight into participants' basic health literacy skills, the Dutch version of the Newest Vital Sign (NVS-D) 13 was administered at the end of each focus group.

| Data analysis
All focus groups were audio-recorded and transcribed. The interviews were analysed using framework analysis by the authors AW and MF. 14,15 In a framework analysis, the first step is to familiarize with the data (familiarization). MF conducted the focus group interviews and AW transcribed and re-read the transcripts. For the second step (thematic analysis), we developed a coding scheme using decision-making stages and health literacy skills as themes using qualitative data analysis software (MAXQDA version 12, VERBI GmbH, Germany). We applied these codes to the focus group transcripts (indexing) and categorized these codes to summarize our findings (charting). This was essentially a comparative process, by which the different transcripts from the individuals eligible for CRC screening and the experts were compared with each other and analysed to find relationships between codes. Agreement on the codes was reached between AW and MF during weekly meetings.

| Characteristics of study population
Of the seventeen experts, all but 1 was born in the Netherlands.
According to the Newest Vital Sign (NVS), 7 of the twenty-two individuals eligible for screening had lower health literacy (NVS score < 4).
Four participants were unable to complete the NVS; 1 was illiterate, 1 reported to have forgotten her reading glasses and 2 participants had to leave before the end of the focus group and were therefore unable to fill out the form.

| Findings from the focus groups in conceptual framework
We used the model by Timmermans 3 and the model by Sørensen 7 as a guide for the analysis of the findings from the focus groups. By integrating our focus group findings within these models, we developed a novel conceptual framework that combines decision-making stages and health literacy skills in the context of CRC screening (Figure 1).
We identified 8 decision-making stages and specified 10 key health literacy skills that were deemed essential for IDM in CRC screening.
These decision-making stages (marked in bold) and health literacy skills (marked in italics) are described in detail below. The selection of quotes that are representative of the decision-making stages and health literacy skills is described in Tables 2 and 3.

| Perceptions of experts Process of decision making and health literacy skills
In general, experts (including scientific researchers and other professionals) stated that the process of decision making about CRC screening starts with receiving the screening information (stage 1). Yet, this was also perceived as being insufficient for making an informed decision. Although the invitation is sent to the invitees' homes via postal mail, experts mentioned the importance of having the skills to actually access the information by opening, reading and understanding the letter. For accessing the screening invitation, experts mentioned that invitees need to identify the screening invitation as being a choice (Quote 1, Table 2). Even though the standard information in the Dutch CRC screening programme was perceived as being sufficient for making an informed decision, experts stated that invitees might search for additional information on CRC screening, for which they would also need the skills to value and judge information. Hence, information about CRC screening, other than the standard information, might also facilitate IDM about participation according to the experts.
With regard to stage 2 (Recognizing that there is a decision to be made), experts pointed out that invitees should at least be aware of CRC screening and understand the information, also to allow making an informed decision about non-participation (Quote 2, Table 2). The decision options were agreed to be participation, non-participation or postponing participation.

Structuring these decision options (stage 3) was believed to be
an essential stage for understanding that the decision to be made is voluntary. In addition to this, experts mentioned that screening invitees need to be able to ask and answer questions about the screening information if they do not understand the information. These were considered to be 2 different abilities. The majority of the experts perceived F I G U R E 1 Conceptual framework of decision-making stages and health literacy skills in colorectal cancer screening structuring the decision options (stage 3) to be an important stage in achieving IDM, yet this was also believed to be the most difficult one, especially when invitees are already aware of CRC screening (Quote 3, Table 2).
In addition, experts from both focus groups mentioned the importance of adding a "knowledge check" for structuring the decision options and outcomes (stage 3). Accordingly, one expert stated that when invitees are about to make a decision, it needs to be checked whether they have really understood the information. This would also "You can inform them so that they apply those skills to make a decision-but they can also put the information aside when, for example, their neighbour has cancer. In this case, they are informed but they do not use the information. "(Shared Decision Making focus group) help invitees to make a decision based on the "right" CRC screening information (Quote 4-5, Table 2). Nevertheless, there was some confusion among the experts about who should perform the knowledge "check" as there is no direct involvement of a health-care provider in the national CRC screening programme. An expert from the shared decision-making focus group eventually stated that there should be a "check" in the CRC screening leaflet (Quote 6, Table 2).
Most experts also mentioned that delegation of the decision (stage 4) to a health-care professional may lead to IDM, provided that screening invitees are able to structure the potential harms and benefits of CRC screening for personal relevance (Quote 7, Table 2).
Furthermore, when screening invitees prefer to delegate their decision (stage 4), they should still be able to understand that there is a decision to be made about participation (Quote 8, Table 2). In all decision-making stages, experts mentioned that screening invitees should also be able to ask for help with reading or translation, especially if they have difficulty understanding the information materials themselves. The involvement of peers, siblings, family and other non-professionals in the decision-making process would then require the ability to value and judge information from others for personal relevance.
Likewise, experts mentioned that invitees might make the decision (stage 6) based on feelings or experiences (Quote 9, Table 2).
This was perceived as being inevitable and not necessarily as something that would lead to a less informed decision (Quote 10, Table 2).
Several experts mentioned that invitees should derive meaning from the screening information for their own situation, which characterizes

stage 5 (Evaluation of these decision options). Hence, in addition to
the ability to understand the information, experts mentioned the importance of understanding risk information and deriving meaning for one's personal situation. Moreover, a number of experts mentioned that even though some screening invitees might have the intention to participate, they may not be able to actually participate (Quote 11, Table 2).
The decision-making stage actual participation (stage 7) was therefore believed to require not only the ability to understand the instructions but also overcoming possible perceived barriers to screening. Experts mentioned that if invitees do have the intention to participate, but are not able to, participation may become a matter of accessibility to

| Perceptions of individuals eligible for screening: Process of decision making and health literacy skills
There  Table 3), yet they could imagine that individuals in their surroundings would discard the letter because they would not recognize this as being important. One participant also pointed out the challenge of uncovering perceptions of individuals that are unlikely to open the screening invitation (Quote 2, Table 3).
For the majority of the participants, participation was self-evident.
Hence, they did not always recognize that there is a decision to be made (stage 2; Quote 3, Table 3). All participants understood that participation was voluntary, yet they did not always understand why peo-  Table 3). A number of participants reported that they would purposely select information from the leaflet, suggesting that the length of the leaflet might be too burdensome (Quote 5, Table 3).
While the experts came up with the following decision options to be structured (stage 3): participate, not participate or postpone participation, the latter was not always recognized as being an option among individuals eligible for CRC screening (Quote 6, Table 3). The vast majority of the participants were positive towards CRC screening (Quote 7, Table 3). Statements concerning evaluating and structuring options and outcomes (stage 3 and 5) often involved consideration of others (Quote 8, Table 3). Some participants mentioned that the decision to participate follows from a moral responsibility towards their family members. Accordingly, a number of participants mentioned that they would participate immediately, without deliberately weighing up the pros and cons of screening.
Although most participants did not mind talking with health-care professionals and informal others about CRC screening, they stated that they would prefer to make the decision about participation on their own. Delegation of the decision (stage 4) to a professional was often dependent on the relationship they had with their health-care provider (Quote 9, Table 3).
While experts mentioned the importance of having the ability to understand and balance risk information for stage 5 (Evaluating the decision options), almost all of the individuals eligible for CRC screening believed that there were no risks involved when performing the FIT (Quote 10, Table 3). By contrast, the follow-up procedure (colonoscopy) was believed to be potentially harmful (Quote 11, Table 3). For some participants, the risk information in the CRC screening leaflet felt too free of engagement, stating that they would like more guidance in what the risks would mean for them personally. Some participants preferred more straightforward information about participation or not, indicating that the information about the pros and cons was too difficult for personal deliberation. In addition, some participants were rather reserved about the provision of further information about the potential harms of CRC screening, as this was believed to discourage participation (Quote 12-13, Table 3). For stage 5 (Evaluating the decision options), a number of participants reported that they preferred to base their decision on factual information rather than on feelings.
Decisions that are based on feelings, rather than on facts, were often believed to result in uninformed decision making. This was exemplified by participants' statements on how the involvement of feelings in a decision-making process may cause distress (Quote 14, Table 3).
Nonetheless, participants' accounts showed that personal values and feelings were naturally present in the decision-making process (Quote 15, Table 3). Participants' decision making was also influenced by their perceptions of CRC risk. For instance, some participants were rather alarmed by the reported risks of CRC in the screening leaflet and mentioned that this would be an important reason for them to participate (Quote 16, Table 3).
All participants mentioned that they understood the instructions for performing the FIT. Even without understanding all the decision options, the participants were confident that they would be able to make a decision themselves (stage 6) and perform the instructions for the FIT. For example, 1 respondent with low health literacy reported that she would ask help from her sister for following the instructions (Quote 17, Table 3). The barriers that were reported in participation were mostly of practical nature, such as costs, collecting faeces and sending the FIT to the laboratory. Nevertheless, those barriers were not considered to be very detrimental in making an informed decision.
All participants were confident that they were able to actually participate (stage 7; Quote 18, Table 3).
Regarding stage 8 (Interpretation of the result), the perceived harms were mostly related to the risks of having complications due to a colonoscopy but not to the risk of receiving a false-positive or false-negative test outcome. Hence, for a number of participants, the potential harms of CRC screening were not always evident (Quote 19, Table 3). This finding also pertains to stage 3 (where the understanding of the information begins) and stage 5 (using this information for the evaluation of the decision options). The idea that CRC screening may cause harm often came as a surprise (Quote 20, Table 3). Only 1 participant explicitly considered the consequences of the test outcomes for undergoing a colonoscopy (Quote 21, Table 3).

| DISCUSSION
We identified and specified 8 decision-making stages and 10 main health literacy skills for IDM in CRC screening and incorporated these within a conceptual framework (Figure 1)

| Strengths & limitations
There are several limitations to this study. First, the majority of the individuals eligible for CRC screening in this study had not been invited for CRC screening yet. The interview questions about decisionmaking processes were therefore mostly hypothetical. However, this also ensured that participants' statements about their decision making were not influenced by screening outcomes. Four participants had already participated in CRC screening. We did not exclude those individuals from participation in our study, as we were interested in the process of decision making and not necessarily in personal attitudes or experiences regarding CRC screening participation. To ensure that we were uncovering perceptions about the decision-making process, MF discussed the information materials with participants at the beginning of the focus group interviews to clarify any misunderstandings.
Accordingly, we tried to mimic the actual invitation procedure by giving participants the invitation materials from the National Institute of Public Health and the Environment (RIVM). It should be noted that our study population is likely to be biased towards people with a positive attitude towards CRC screening and may therefore report fewer barriers to CRC screening. With regard to the focus groups with experts, it is important to mention that most professionals are experts in the field of shared decision making (SDM), in which the health-care provider plays an important role. Even though the experts were well aware of the differences between SDM and IDM, this sometimes led to confusion as there is no direct involvement of a health-care provider in the national CRC screening programme.

| CONCLUSIONS
This study provides insight into the decision-making stages and its corresponding health literacy skills that are essential for IDM in CRC screening. Our findings show important differences in perceptions between individuals eligible for CRC screening and experts on these decision-making stages and skills. The conceptual framework can be used to inform the development of context-based measurement of health literacy and interventions to support IDM in cancer screening.