Patient and Public Involvement in Inflammatory Bowel Disease Research—A Scoping Review

Abstract Background Interest in patient and public involvement in research has grown. Medical, health, and social care research has demonstrated several benefits of patient and public engagement, such as empowering user input and reducing attrition rates in clinical trials. To date, no study has reviewed patient engagement in inflammatory bowel disease (IBD). We aimed to describe the benefits, challenges, and best practices of patient engagement in IBD research. Methods We performed a systematic search on MEDLINE, EMBASE, and Cochrane for all clinical IBD research studies in which patients were involved in the research process (1946- 2023). Patient input was considered in: (1) study design, (2) study execution, (3) research dissemination, and/or (4) other domains not specified here. Two authors independently screened and extracted data on type of engaged person(s), format of engagement, author-reported benefits, recommendations, and challenges. For each study, we reported the level of patient engagement and study adherence to standardized reporting guidelines. Results After screening 9,355 articles, we included 51 for final analysis. IBD patients were most frequently engaged in study design. Patient engagement in IBD research improved recruitment rates and promoted the creation of user-friendly quality-of-life tools. Selection bias and recruitment difficulties were common challenges in the application of patient engagement. Authors recommended continuous patient involvement to address emerging priorities and cognitive interviewing to improve questionnaire clarity. Conclusions Patient engagement represents an important step in promoting patient-centred care. According to study authors, implementing cognitive interviewing techniques, continuous patient involvement, and standardized reporting guidelines may improve future iterations of engagement in IBD.


Introduction
Interest in patient and public involvement (PPIn) in research has grown. 1 An early example of patient involvement occurred in the 1980s in the UK, wherein patient group representatives conducted a trial on chorionic villous sampling in pregnancy. 2takeholder engagement has also been adopted in social and healthcare research in the UK, where the INVOLVE project supports active public involvement in the National Health Service (NHS). 3 Since then, there has been a growing emphasis on engaging patients in research directly related to their care. 4esearch in health and social care has demonstrated several benefits of PPIn. 5,6These include empowering user input and providing researchers with a greater understanding of community perspectives. 6In medicine, PPIn has been demonstrated to positively impact patient enrolment in clinical trials. 1 On ethical grounds, engaging patients in research relevant to their care may democratize the research process. 7o date, no study has comprehensively reviewed patient engagement in inflammatory bowel disease (IBD) research.IBD is a chronic disease with a significant burden on patients' personal, social, and occupational functioning. 8IBD patients frequently play an active role in their disease management. 8As such, IBD patients may be able to offer their knowledge to research studies as experience-based experts.
In this scoping review, we analyzed studies that actively involved IBD patients (and other relevant stakeholders) in research.Using a meta-narrative approach, 9 we aimed to provide a synthesis on implementing patient engagement in IBD and to address the following questions: How and during what stage of research are IBD patients engaged?What are authorreported recommendations for best practices of PPIn in IBD?What are the benefits of PPIn in IBD?What are the challenges (and suggested solutions) of PPIn in IBD?

Methods
We comprehensively reviewed IBD research studies in which patients were active participants in the research process.Reporting of our findings followed guidelines for the reporting of scoping reviews (PRISMA extension for Scoping Reviews). 10A completed checklist of the reporting guidelines can be found in Text, Supplementary Data Content 1.

Search strategy
We ran a systematic search in EMBASE, Medline, and the Cochrane Central Register of Controlled Trials for clinical IBD research studies in which patients were actively involved in research.The following study types were considered for inclusion: clinical practice guidelines, randomized controlled trials, cohort studies, cross-sectional studies, systematic reviews, meta-analyses, survey studies, cost-effectiveness analyses, and qualitative studies.We excluded opinion pieces, editorials, abstract-only submissions, research letters, case reports/series, and protocol-only entries.We only included articles published in English.The search was not limited to specific countries.The search was designed by a librarian.The search strategy was also peer-reviewed and assessed against the Peer Review of Electronic Search Strategy (PRESS) checklist. 11The searches were run from inception to August 21, 2023.The full search strategies can be found in Text, Supplementary Data Content 2.

Study selection
Two authors independently reviewed the abstracts (K.E., E.N.) and full texts (K.E., A.L.) for eligible studies using the screening platform Covidence.Discrepancies were resolved by consensus.Patient input was considered in: study design (prioritization of research topics, outcome selection, study tool development, and funding acquisition); study execution (study recruitment, data collection, and analysis); dissemination of research (manuscript development); and/or other domains not specified here.Engaged person(s) included IBD patient(s), and/or other stakeholders (patient representatives, caregivers, and community members).

Data extraction
Two authors extracted the following data from full texts: article type, study objectives, research setting, enrolment method(s), sampling method(s), engaged person(s), and method(s) of PPIn, which included focus groups, semistructured interviews, surveys, and/or multidisciplinary panels.Where possible, we sorted instances of PPIn into one or more of the following categories: study design, study execution, and/or dissemination of results.
For each instance of PPIn, we obtained a narrative description of patient contributions from the study article.We searched each full text for author and patient-reported best practices, benefits, challenges (and suggested solutions) of PPIn.We reported level of patient engagement according to the Patient-Oriented Research Level of Engagement Tool (PORLET) and adherence to standardized reporting guidelines according to the Guidance for Reporting Involvement of Patients and the Public, Version 2 (GRIPP2) for each study. 12,13

Analysis
Quantitative data on article type, engaged person(s), method(s) of engagement, and stage of patient engagement in the research process was summarized using descriptive statistics.The qualitative data were analyzed using a meta-narrative approach, adopted from Domecq et al. 7,9 Following a literature search with clear selection criteria, the approach adheres to a framework defining four key questions (methods, best practices, benefits, and challenges of PPIn).As per the framework, we reviewed narrative data from each article and synthesized key themes, using specific studies to highlight themes and map available evidence.Specifically, we reviewed the Discussion section of each article for methods, benefits, challenges, and best practices of PPIn as identified from prior literature, 7,14 and extracted any additional themes reported by the authors.
The most frequent form of PPIn was patient consultation in the development of IBD study tools, including questionnaires, guidebooks, and a video animation (n = 44, 86.3%).A qualitative study exploring disclosure of IBD among children utilized a core e-Advisory group of IBD patients to provide insight into young people's experiences with disclosure, 23 which informed the development of a two-minute animation. 23BD patients and their surrogates also acted as active participants in study recruitment in four studies (7.8%). 15,35,52,65n one study, patient champions within the project team devised a new method of identifying and transferring IBD patients to specialist nurse-led telephone clinics, which helped boost transfer rates. 30ther modalities of PPIn included assisting with data analysis (n = 8, 15.7%), wherein one study provided patients with training in qualitative analysis methods from an experienced qualitative researcher. 29Six studies (11.8%) included patients and/or other stakeholders (e.g., patient advisors) as co-authors on the published work.Of note, one study on the development of an IBD transfer toolkit was spearheaded by an IBD patient, who acted as the lead study author in collaboration with a paediatric gastroenterologist. 41This was achieved by involving the patient partner from the outset of the project in study design.One retrospective study directly cited engaged patients' reflections on study results in their discussion, including their thoughts and assessment of the increasing prevalence of IBD among First Nations. 64dherence to reporting guidelines for PPIn was evaluated via the GRIPP2 checklist (Table 2).All studies in our cohort (n = 51) reported the methods used for PPIn.Twentyfive reported the aim of PPIn, 35 reported results of PPIn, 32 reported positive and/or negative effects of PPIn, and 19 commented critically on PPIn in the study (reflecting on positive experiences and/or areas of improvement).
A pair of studies linked to a patient-oriented research initiative achieved a high level of engagement. 52,65One study evaluated perspectives of healthcare use among rural Canadians with IBD. 52The study engaged patient and family advisors as equal members in decision-making.This was achieved by engaging patients in all phases of the research process.Patient partners contributed to the study design, co-created recruitment materials, reviewed findings, and co-developed the manuscript. 52,65A separate study with high patient engagement compared healthcare utilization between First Nations patients and the general IBD population.This retrospective cohort study involved indigenous patients in study outcome selection, data analysis, and the knowledgesharing phases of research (wherein 1 advocate co-presented the published work at multiple conferences). 59This was mediated by sending the engaged parties periodic reports and requesting regular feedback on results. 59at are author-reported recommendations for best practices of PPIn in IBD?
Three IBD studies in our sample (5.9%) cited the importance of recruiting patients broadly for PPIn. 15,24,36In one study, authors noted that recruiting patients from a wide variety of centres and different regions of Spain helped ensure the generalizability of their findings. 29Two studies (3.9%) encouraged cognitive interviewing with patients as a tool in questionnaire development, with a validation study noting it improved question clarity, ease of understanding, and increased item validity. 38,47Last, a study engaging IBD patients in online survey development recommended continuous patient  involvement to address patients' emerging concerns during clinical testing. 54at are the benefits of PPIn in IBD?
The most reported benefit of PPIn, cited across 21 studies (41.2%), was that it helped promote patient-centred care and/or ensured that the patient voice was represented.In one study soliciting research uncertainties in the management of pediatric IBD, authors highlighted the role of patient engagement in establishing a research agenda that was mutually impactful to both those treating and those experiencing the disease. 31 second theme centred on the role of PPIn in strengthening the relevance and/or credibility of study items.Authors of a quality-of-life questionnaire for household members of IBD stated that involving IBD stakeholders in the development of their tool helped focus items on issues most relevant to responders. 55Lastly, a tertiary benefit reported by one study was that patient engagement promoted the creation of a user-friendly and understandable quality-of-life tool in IBD research. 19at are the challenges (and suggested solutions) of PPIn in IBD?
Two studies (3.9%) cited feasibility as a challenge to incorporating PPIn in IBD research, specifically as it relates to recruiting and engaging participants as part of study design. 25,56n a study testing a decision aid encompassing reproductive decisions in IBD, authors made note of intrinsic difficulties with patient recruitment for PPIn, related to the time required to conduct patient focus groups and guide the development of the decision aid.This was cited as a challenge in recruiting patient participants, especially young patients who may have professional commitments and/or time constraints related to family.56 Another challenge identified across 4 studies (7.8%) was that engaged patients may not be representative of the entire IBD population.One study highlighted a lack of diversity in education and literacy among focus group participants.42 The authors of a quality-of-care questionnaire developed by Swedish IBD patients stated that the use of the questionnaire may be limited to a Swedish care context.38 These authors recommended cultural adaptation of the tool if it were to be used in a different context.

Discussion
In our analysis of 51 original articles involving patients and/ or other stakeholders in IBD research, we found that IBD patients were most frequently engaged in the design phase of the research process.Across three studies, they were involved in setting IBD research priorities.The influence of PPIn on the research agenda has previously been reported in a review of INVOLVE, a publicly funded NHS patient involvement project. 14Several studies in the review demonstrated that PPIn led to clearer research priorities, a wider set of topics being considered, and a shift in research focus to be more in line with public concerns. 14,66More recently, a summative report on the impact of IBD in Canada incorporated patients' and caregiver partners' perspectives on several research articles. 67The goals of this engagement were to define key advocacy priorities for an IBD patient organization and to highlight content within the report that was most relevant to IBD patients. 67 one study by McCormick et al., the involvement of women with breast cancer in environmental causes research shifted the focus of the program from a biochemical model to a political one that better reflected the women's interests. 68PIn was also cited to enhance the credibility of IBD study tools.This effect has been demonstrated in community and social care research, where evidence suggests public engagement gives both the researchers and the research project greater credibility. 7,69For instance, in a research study involving Alaska Natives, community members outperformed researchers in recruiting participants.This was attributed to community members giving legitimacy to claims the project was being conducted in partnership with the community. 70everal factors may explain the observed role of PPIn in improving research enrolment.First, as seen in three studies in our cohort, patients may act as active participants in study recruitment, directly supporting the efforts of study authors.Second, patients may indirectly support study recruitment via contributions to research design.Authors of a pediatric RCT on osteopathy attributed the trial's high enrolment rate to the stakeholders' contributions to group design. 71A RCT on environmental control education in asthma similarly acknowledged the role of a community advisory board in promoting successful recruitment strategies, along with creating study reports that were understandable to the community. 72ith these benefits in mind, the costs of PPIn, along with recruitment difficulties, may limit the feasibility of incorporating PPIn in IBD research.A literature review by Shah et al. cited time constraints as a key impediment to involving users in the development and evaluation of medical device technologies. 73,74PPIn likely represents a significant time commitment for patients and researchers, which may hinder its widespread application.The profile of engaged patients may also differ substantially from that of the general IBD population.Viswanathan et al. ( 2004) cited a recruitment bias toward highly motivated people in research involvement.In the IBD cohort, such a bias might hamper the applicability of certain quality-of-life interventions, which often require significant investment on the part of the patient. 5tudy heterogeneity in our sample limits our synthesis of patient engagement in IBD.Best practices of PPIn are likely to vary with the context of engagement.Nevertheless, we outline the following recommendations for implementing participatory research frameworks in IBD.(1) We recommend recruiting engaged parties broadly to ensure findings are generalizable to the IBD population.(2) With time commitment being a key limitation in recruitment, we encourage researchers to elicit regular patient feedback to modify the involvement process in accordance with patient needs.(3) When engaging patients in questionnaire development, we propose employing cognitive interviewing techniques to improve individual item clarity.(4) We recommend engaging patients continuously throughout the research process to address emerging concerns.This is consistent with prior research from Lindenmeyer et al. and Rhodes et al., who found long-term involvement aided user-researcher cohesion and facilitated a deeper knowledge of and contribution to the research process. 69,73 (5) We recommend authors adhere to reporting guidelines for PPIn such as PORLET and GRIPP2 to better define the scope of PPIn and standardize its methodology.
In addition to the above recommendations, the Canadian Institutes of Health Research has designed a framework highlighting guiding principles, and core areas patient

Table 1 .
Study characteristics and level of engagement according to Patient-Oriented Research Level of Engagement Tool (PORLET) criteria (n = 51).

Table 2 .
PPIn according to guidance for reporting involvement of patients and the public, version 2 (GRIPP2) reporting checklist (short form) (n = 49).