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Original Articles: Gastroenterology: Inflammatory Bowel Disease

Engaging Patients and Caregivers in Research for Pediatric Inflammatory Bowel Disease: Top 10 Research Priorities

Grant, Amy; Crane, Melissa; Laupacis, Andreas; Griffiths, Anne; Burnett, Dave; Hood, Amanda§; Kluthe, Cheryl||; Maghera, Muneet§; Mann, Malcolm§; Mansi, Melissa§; Murray, Kate§; Trempe, Marie-Josée; Otley, Anthony∗,#

Author Information
Journal of Pediatric Gastroenterology and Nutrition: September 2019 - Volume 69 - Issue 3 - p 317-323
doi: 10.1097/MPG.0000000000002396

Abstract

What Is Known/What Is New

What Is Known

  • Engaging patients in research contributes to the increased applicability, quality, and knowledge translation of research findings.
  • Historically, research topics have been driven by available funding and researcher interests.
  • The James Lind Alliance has developed a standardized approach to identify and prioritize research uncertainties from patients and stakeholders to identify relevant topics that have not yet been addressed.

What Is New

  • A list of the top 10 shared research priorities of patients, caregivers, and clinicians in pediatric inflammatory bowel disease was identified.
  • The cause and prevention of inflammatory bowel disease, and the role of diet were amongst the top prioritized questions.

Health research priorities are traditionally chosen by individual researchers and industry with little to no patient input (1). Given the differing perspectives of patients and clinicians, clinical practice and outcome measurement may be markedly different if patients are consulted in the research process (2,3). The impact of the patient voice is exemplified in previous research, whereby patients with arthritis reported fatigue as their most highly ranked symptom, not pain as suspected by clinicians (4). Without the inclusion of patients, fatigue was previously overlooked. If those with lived experience are not included in research priority setting, it is likely that some research topics that patients and caregivers deem important will not be addressed.

In order to hear from those with lived experience, we engaged pediatric patients, family members of pediatric patients, and clinicians who care for those with inflammatory bowel disease (IBD) to identify and prioritize unanswered research questions in pediatric IBD. IBD manifests during childhood or adolescence in 20% to 25% of patients (5), with Canada having among the highest reported prevalence and incidence rates of IBD in the world (6,7). Thus, the Canadian population has a wealth of relevant lived experience related to the treatment and management of pediatric IBD, which present unique social (eg, use of a nasogastric tube for tube feeds, side effects of steroids on appearance) and growth challenges (8). Although the treatment and management of IBD has similarities across both pediatric and adult care, there are unique aspects to pediatric IBD which are not appropriately captured when an adult lens alone is used.

The aim of this study was to solicit the 10 most important research uncertainties in the management of pediatric IBD from the point of view of patients, caregivers, and clinicians using the James Lind Alliance (JLA) approach to research priority setting (9–12).

METHODS

We used the JLA framework (12) involving patients, caregivers, and clinicians throughout the priority-setting process. This framework has been used for over 10 years to prioritize research uncertainties or unanswered research questions in numerous conditions. The process will be briefly described here, but this is further described in Supplemental material (Supplemental Digital Content, http://links.lww.com/MPG/B655). Additional research using the JLA framework can be found at http://www.jla.nihr.ac.uk/.

The JLA process involves forming a steering committee of patients, caregivers/family members, and clinicians, who inform and are directly involved in the research processes associated with the solicitation of unanswered questions from the community. The research team, which involved all members of the steering committee, created an online survey to capture uncertainties around the treatment and management of pediatric IBD. These recruitment methods were chosen due to high accessibility from both teenagers, and parents (13–15). This survey was advertised through local networks (ie, IBD-specific Facebook groups, community organizations involved in IBD support), pediatric IBD clinics, and national IBD organizations. In addition, 2 in-person focus groups were held to solicit research priorities from younger pediatric patients (age 6–12 years), as they would have more difficulty accessing and answering an online survey independently.

The survey was advertised broadly, and closed once we felt there was fair representation from the 3 main groups of respondents (clinicians, patients, and caregivers), taking into account age, sex, and type of health professional. Questions submitted from surveys were combined with focus group responses and questions abstracted from a review of clinical practice guidelines. Qualitative analysis of the questions submitted took place using NVivo Software (16). Items were categorized into themes (17,18) using the methodology reported by Manns et al (17). The steering committee worked in clinician-patient/caregiver pairs to form indicative questions by combining similar questions and removing redundant items or questions out of scope. These questions were subsequently divided into those “with an answer” and those “without an answer” in the scientific literature.

These unanswered questions were then put into a final national survey, which was again disseminated across Canada. Participants were asked to rank their top 20 research questions in decreasing order of importance. After the survey was closed, priority scores were calculated, and a group of highly ranked items was brought forward to the final prioritization workshop.

This prioritization workshop was held to complete prioritization, following the JLA process (12). A nominal group technique (12,19) was used to help participants organize their personal priorities ahead of the workshop. Three experienced facilitators, who did not have personal or professional experience with IBD, led small group discussions. The groups deliberated on the rank order of items through 2 separate small group discussions along with large group ranking, until consensus on the top 10 research uncertainties was reached.

Ethics

Local ethics approval was obtained at each participating site, where required. Given the anonymous and publicly accessible nature of the survey, and use of implied consent (hitting submit on the survey implied consent, and was indicated as such), some ethics boards did not require ethics approval (n = 9). Others required approval (n = 3) as information about the study was disseminated and distributed within clinical practice areas.

RESULTS

Soliciting Uncertainties

A total of 363 respondents reported a total of 1209 research uncertainties (Fig. 1). Respondents included 111 patients who developed IBD before 18 years, 133 caregivers, and 46 interdisciplinary health professionals, along with an additional 73 respondents (Table 1). A portion of the sample came from focus groups, which were held in Halifax, Nova Scotia and Edmonton, Alberta. This subsample included 7 pediatric patients, 12 caregivers, and 2 siblings. Discussions were facilitated with caregivers and patients separately, using a guideline that reflected the same topics as the online questionnaire. Focus group transcripts were added to the overall bank of survey data.

FIGURE 1
FIGURE 1:
Research process of soliciting and prioritizing research uncertainties.
TABLE 1
TABLE 1:
Demographics from completion of 2 national surveys

After reviewing the questions generated, the list was condensed to a total of 626 unique questions which were subsequently divided into 17 themes through qualitative analysis of the data (Table 2 themes, and number of questions within each theme). After a review of the literature, 388 questions were considered “unanswered” and in scope. Examples of questions that were out of scope included questions referring to the adult population, such as “How much will I flare when I am an adult,” or those that refer to broader topics, such as general diet “Are there any drugs that I can take so that I don’t react to milk?” The in-scope unanswered questions were sorted by theme, with major themes including diet (n = 54 questions), treatment (n = 51), emotions (n = 42), and cause (n = 34). Each steering committee clinician-patient pairs (or triads) formed indicative questions within several themes, resulting in 73 remaining questions. An additional 46 questions were identified in a thorough review of the literature and clinical practice guidelines, 32 of which were relevant to pediatric patients with IBD. For example, the question of whether the use of fecal calprotectin to infer IBD activity can reduce the need of endoscopy was included (20). The additional 32 questions were added to the overall question bank, resulting in 105 unanswered, indicative uncertainties that were within scope.

TABLE 2
TABLE 2:
Number of unanswered research questions by theme, before and after interim prioritization

Interim Prioritization

Patients (n = 25), caregivers (n = 20), and interdisciplinary health professionals (n = 30) completed the online ranking survey (Table 1). The rank of each generated response was reverse scored (ie, a rank of 1 was scored as 20, a rank of 20 was scored as a 1), and scores were summed for each question across respondents (12). Sum scores were computed separately for patients/caregivers and clinicians to recognize and examine differences in ranks between groups (Table 3). Scores were, however, summed across both groups to generate a total summed score, which was used to make decisions on the most highly ranked items to be further prioritized in the next stage. Many of the questions were similarly ranked across patient/caregivers and clinicians, whereas others had differences in ranks. For example, “What are the causes of IBD” was ranked as number 1 across all groups, conversely clinicians ranked the best approach to transitioning from pediatric to adult care higher (ranked 8th) than patients/caregivers (ranked 32nd). Given that the JLA process represented shared decision making by all those with lived experience, or experience treating those with pediatric IBD, the collective rank was used to determine the most highly ranked items. A natural cutoff occurred after the top 27 questions, and therefore these questions went on to the final prioritization workshop. These 27 questions were distributed across 12 of the initial 17 themes (Table 2).

TABLE 3
TABLE 3:
Top 27 research uncertainties with patient/caregiver, clinician rank, and final rank after the national prioritization meeting

Final Prioritization

Before the workshop, the 10-member steering committee met to review the top 27 uncertainties, and to decide on any final changes to the list of unanswered research questions (Table 3). After deliberating, the committee removed 5 of the uncertainties by combining them (ie, adding detail, seeing an overlap in content) into other existing indicative questions, and formed 2 new indicative questions on diet by combining the 5 diet questions in the original 27-item list, leaving 19 uncertainties that entered the final workshop. The prioritization workshop was attended by the steering committee, and 2 additional patients, 4 caregivers, 1 sibling, and 5 clinicians. The clinicians attending the workshop were gastroenterologists (n = 3), nurses (n = 2), dietitians (n = 2), a social worker, and a psychologist who all worked directly with pediatric patients with IBD. Workshop attendees came from provinces across Canada. After a day of small-group and large-group deliberations, the final top 10 questions were agreed upon by all 21 attendees (Table 4).

TABLE 4
TABLE 4:
List of the top prioritized research questions in pediatric inflammatory bowel disease (1–18)

The group listed “What are the causes of IBD” as the number one ranked question to guide future research in pediatric IBD. This question was formed as an indicative question based on question solicitation from the first national survey, which included questions such as “can environmental factors cause IBD,” “is there a gene associated with IBD,” and “why did [IBD] happen in one of my kids but not the other?.” The second most highly ranked question asked “can IBD be prevented?” was formed from original questions such as “what can be done during the maternal stage to prevent offspring from getting IBD?”. The third most highly ranked question was “what role does diet have in the management of pediatric IBD,” which was formed from the theme with the most questions submitted in the national solicitation survey, showing that this is of high importance to patients, caregivers, and clinicians. The remaining top 10 questions are shown in Table 4.

DISCUSSION

This priority setting partnership identified the top 10 shared research priorities of Canadian patients, caregivers, and clinicians in pediatric IBD. “What are the causes of IBD?” was ranked as the top question. Research about the role of the gut microbiome, genetic predisposition, diet, and environment is ongoing (21–23), but we still do not fully understand the cause of IBD. Understandably, this was also the highest ranked and most frequently reported question from the national survey. Emphasis was put on prevention of IBD, and in some contexts, how to prevent IBD in potentially susceptible populations (eg, in geographic areas where IBD is prevalent, or in siblings of children with IBD). Diet was a pervasive topic where it was frequently reported by respondents and included the role of diet in cause/prevention, management, and treatment of IBD. Exclusive enteral nutrition has been found to be an effective dietary intervention in pediatric patients with Crohn disease, in that it effectively induces remission and has fewer side effects than other treatments (eg, steroids) (24,25). The effectiveness of enteral nutrition as a long-term treatment is, however, less studied, and there are large variations in use of this dietary therapy globally (26). Researchers have yet to find a diet with long-term effectiveness that works in all patients with IBD (eg, in ulcerative colitis) (22).

This research presents the unique perspective of pediatric patients, which complements the JLA advised priority setting partnership completed in the adult IBD population in the UK (27). Some of the unique concerns identified in the pediatric population included lifelong psychosocial factors, long-term effect of the disease and treatment, and considerations about transition to adult care. There were also some similarities in items prioritized in the adult and pediatric populations around the need to understand the best treatment, including diet, to keep IBD symptoms in remission. In addition, both groups identified optimizing markers of disease, such as endoscopic assessment, and other less invasive biomarkers to better understand the disease at diagnosis and throughout the disease course.

In addition to contrasting the current pediatric focused results to the adult IBD priority setting process, it was interesting to examine the similarities and unique differences across the groups with respect to ranking. For example, clinicians ranked the question around transitioning from pediatric to adult care higher than patients/caregivers, whereas patients/caregivers ranked the question around the effects of an early diagnosis of IBD on lifelong course of the disease much higher than clinicians. In contrast, the top 5 items were ranked similarly across these 2 groups, which included questions around the cause, prevention, susceptibility, and questions around diet. This highlights the importance of engaging all stakeholders in the research process.

The JLA process creates a list of “shared” priorities with clinicians, patients, and caregivers working together to reach a consensus on research questions of importance. The process values the opinions of all those with lived experience in a specific disease group. With this in mind, our research team was very cognizant of the typical dynamic that patients and clinicians have, and considered this at the outset of the project through rapport building, and ensuring team members were comfortable voicing their opinions and speaking up in a group. During the final prioritization workshop, each group was presented with information on how many patients, clinicians, and caregivers submitted questions related to the indicative question they were considering and were instructed to intentionally consider this in their decision making to ensure that the views of all groups were represented. Anecdotally, we were astounded by how articulate, and vocal all of our nonclinician representatives were (pediatric patients, caregivers). By engaging current pediatric-aged patients, along with young adults who were diagnosed at a pediatric age as equal partners on the project steering committee, the pediatric patient voice was represented. A teen with IBD served on the steering committee, as did 2 parents of young children with IBD. The JLA has found that caregivers can provide some insight into the perspectives of younger children (18). Since younger participants were thought to be less likely to complete the online questionnaire, focus groups included participants as young as 6 years old, so that this group's uncertainties were included. In general, the uncertainties raised during the focus groups aligned with those from the survey.

Priority setting processes are an opportunity to understand the questions that do not have an answer in the scientific literature, and those that do have an answer but appear unknown to those who submitted them. Some common examples of the latter included the difference between Crohn disease and ulcerative colitis, and questions about the link between IBD and colon cancer, for which there is much published data and supported mechanisms of causality (28–31). Identifying and recognizing these common questions is vital to ensuring that patients and families are aware of the options in treating IBD (32,33). By understanding trends in these answered questions, we can help to bridge potential gaps in knowledge or in the distribution of educational resources to patients, families, and perhaps even clinicians. The importance of continued engagement with patients and families through the knowledge translation of these materials is vital to ensure that the materials produced are of value to patients, and in a format that will have good uptake for those interested (34,35).

As a next step, our team is currently developing educational stop-motion videos and accompanying infographics about the results of this process. The first video will be about the research prioritization process and the resulting research priorities identified. The second involves a subset of the answered research questions identified, to help in knowledge translation. The steering committee is working with organizational partners to disseminate these materials using social media, and through the clinics and organizations that pediatric populations frequent. Having gained an understanding of these shared research priorities, the next steps are to work with IBD partners to disseminate these findings to researchers and funders to prioritize the funding of research that will seek answers to these uncertainties. This work contributes to a considerable shift in the research community, where patients are engaged as partners in research.

Inherently, there were also some limitations to the current work. Although our group attempted to be inclusive via a national survey, and to ensure broad representation across sex, type of IBD, age of patients, and to include many groups of health professionals, we recognize that certain groups of patients and/or professionals were underrepresented due to limitations imposed by time, geography, and known issues with recruitment of research participants. Increased engagement with these underrepresented groups (eg, patients of low socioeconomic status patients who have less opportunity to participate in a volunteer-based activities) in future work is needed (36,37). By using the established and rigorous, mixed-methods JLA process, some of the bias associated with identifying research priorities was reduced. We, however, acknowledge that subjectivity is still very much at play, as the consensus process is informed by the participants present, and would likely result in a different list of ranked priorities if repeated with a different group of participants. Despite these limitations, we do feel that the broad dissemination of the initial solicitation survey across Canada, targeted recruitment of patients, caregivers, and various types of clinicians to participate in the final priority setting workshop in addition to use of neutral facilitators resulted in a selection of research priorities that represent a group of shared research priorities.

Patient input into the research process is becoming increasingly valued within the healthcare system. The idea that patients should be treated as passive subjects in their care, or the research that goes into improving care, is changing. Patients and families have the potential to make significant contributions to research as active research participants; given the opportunity, they can engage in all stages of the research process. Research is starting to show that engaging patients in research results in improvements to the quality of research, which range from identifying symptoms that have the most impact on patients, identifying true treatment uncertainties, to improving the likelihood of recruiting to target (3,38–41). This project represents the first formal attempt to engage patients and families in research as active participants in the Canadian pediatric IBD population.

Acknowledgments

The authors would like to thank the Canadian Children Inflammatory Bowel Disease Network (CIDsCANN): A Joint Partnership of CIHR and CH.I.L.D. Foundation team of investigators and research staff across Canada for supporting and participating in this research, including investigators: Dr Thomas Walters, Dr Kevan Jacobson, Dr David Mack, Dr Wael El-Matary, Dr Jeffrey Critch, Dr Hien Huynh, Dr Jennifer De Bruyn, Dr Colette Deslandres, Dr Ernest Seidman, Dr Kevin Bax, and Dr Mary Sherlock. This work was funded by the Canadian Institutes for Health Research (CIHR) SPOR Patient Engagement Collaboration Grant, in partnership with Abbvie. Thank you to the SPOR IMAGINE Network for their partnership. Special thanks to the patients, families, and clinicians who participated in this national survey and in the final priority setting meeting, as without your time and contribution, we would not have been able to complete this work.

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Keywords:

Crohn disease; inflammatory bowel disease; patient engagement; pediatric; priority setting; research priorities; ulcerative colitis

Supplemental Digital Content

Copyright © 2019 by European Society for Pediatric Gastroenterology, Hepatology, and Nutrition and North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition