Older adults are underrepresented in clinical cancer research.1–7 Evidence shows that engaging patients in the research process can lead to increased enrollment and retention rates8–11 and enhanced credibility of the findings, which in turn increases translation of research into clinical practice.12 Patient engagement in research is expected to lead to improved health outcomes and better uptake of findings because the research is expected to be more relevant for patients.13 Stakeholder participation in determining crucial areas of research and healthcare services has been recognized in the United Kingdom by the British National Institute of Health since 1996, leading to the project INVOLVE.14 Additionally, the US Patient Centered Outcomes Research Institute (PCORI; established in 2010) strongly emphasizes the importance of stakeholders and patient engagement in the research process.15,16
There is also a movement in Canada to engage patients in research. Patient engagement has been defined by the Canadian Institutes of Health Research as “meaningful and active collaboration in governance, priority setting, conducting research and knowledge translation. Depending on the context, patient-oriented research may also engage people who bring the collective voice of specific, affected communities.”13
Despite the increasing requirements of funding agencies to engage patients on research teams, there are few data to suggest the most effective approach.8 Additionally, there is a paucity of research on what older adults with cancer (OAWCs) see as research priorities for cancer, how they feel about being research team members, and what supports and resources they require to participate in this process; this is important to examine because engagement can lead to patient frustration.17
The goals of this study were to understand the research priorities of OAWCs and their caregivers, and examine how OAWCs and their caregivers can be engaged in research teams and what supports are needed.
Methods
Study Design
This study was designed with OAWCs and caregiver representatives on the team and was conducted in 2 phases (Figure 1): public meetings followed by focus groups. At the end of each phase, participants were invited to join the participant panel aimed at engaging them to be on a future research team.
The study was approved by the Research Ethics Board of the University of Toronto. All participants provided consent before participating in the surveys and focus groups.
Participant Recruitment
Partners for this project included hospitals in the region, health charities, and advocacy organizations for patients and older adults. For the public meetings and focus groups, older adults aged ≥60 years who had been diagnosed with any type of cancer in the past 10 years and their caregivers were recruited separately using several strategies, including study Web site; recruitment posters and business cards in oncology waiting areas in partner hospitals and senior
Study timeline and participant flow through the phases of the study.
aDue to anonymity in the survey, as well as a few incomplete surveys, we could not determine precisely how many participants in the participant pool came from phase 1, phase 2, or both.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 15, 10; 10.6004/jnccn.2017.0159
Study timeline and participant flow through the phases of the study.
aDue to anonymity in the survey, as well as a few incomplete surveys, we could not determine precisely how many participants in the participant pool came from phase 1, phase 2, or both.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 15, 10; 10.6004/jnccn.2017.0159
Study timeline and participant flow through the phases of the study.
aDue to anonymity in the survey, as well as a few incomplete surveys, we could not determine precisely how many participants in the participant pool came from phase 1, phase 2, or both.
Citation: Journal of the National Comprehensive Cancer Network J Natl Compr Canc Netw 15, 10; 10.6004/jnccn.2017.0159
Attendees who needed transportation arrangements were provided with taxi services to and from the venue for both public meetings and focus groups, and lunch was provided.
Public Meetings
Three public meetings were held to better understand the research priorities of OAWCs and caregivers. The public meetings took place on Saturdays at 3 different University of Toronto locations in September, October, and November of 2015 and lasted for 3 hours, with half an hour for a reception and farewell. Research priorities were identified in small group discussions and notes were taken by nursing students. The research priorities from the public meetings were summarized.
Surveys were administered at the end of the public meetings to measure satisfaction, understand how to improve future meetings, and invite OAWCs and caregivers to participate in a focus group and join the participant pool. The survey collected information on age, sex, education level, cancer diagnosis, years since diagnosis, and self-rated health. Completion of the survey was voluntary.
Focus Groups
Focus groups aimed to explore what OAWCs and caregivers felt about being co-researchers on the team and to identify supports needed to enable/facilitate older adults and caregiver participation as research team members. The 7 focus groups were held in public libraries across the GTA from December 2015 through April 2016 and lasted 2 hours. All focus groups included both OAWCs and their caregivers in the same group, and were moderated by an experienced moderator and audio-recorded (a guide with the moderation questions is provided in supplemental eAppendix 1, available with this article at JNCCN.org). A second member of the research team took notes. At the end of the focus groups, participants were asked to complete the survey, which was voluntary. Participants were also invited to join the participant panel. The number of focus groups was determined based on data saturation (eg, no new themes emerged).
Data Analysis
Survey responses were entered into a Microsoft Excel spreadsheet and descriptive analyses (frequencies, median, and range) were used to describe the characteristics of the participants.
The audio recordings from the focus groups were transcribed verbatim and the content then analyzed, along with the handwritten field notes using thematic content analysis.18–20 The team explored and identified emerging themes through reading and coding the focus group transcripts and notes taken by team members. The findings of OAWCs and caregivers were analyzed together because the discussion was held together, and no differences in answers were noted by the team members. A summary of the findings of each focus group was sent to each participant with a prestamped return envelope. Participants could correct the findings, add missing information, and return the modified summary to the research team as a form of member checking.
Results
Public Meetings
Table 1 presents a description of the participants. A total of 33 OAWCs and 19 caregivers attended a public meeting. Although 29 OAWCs completed at least part of the survey, only 26 (79%) answered the sociodemographic questions. The median age for OAWCs was 71 years; most (n=23; 79%) lived at home and one-third (n=9) lived alone. A total of 17 OAWCs (60%) rated their health as “good” or “excellent”; 9 (31%) were receiving some form of active cancer treatment.
The median age of caregivers was 71 years; 11 were a spouse or partner. All respondents had a high school education or higher. The median number of caregiving was 3.5 years (range, 0–21 years), and 13 caregivers (76%) considered their health to be “good,” “very good,” or “excellent.”
Research Priorities of OAWCs and Caregivers
Table 2 lists the research priorities identified by OAWCs and caregivers at the public meetings. The most commonly voiced priorities were finding a cure for the disease and integrating complementary and
Sociodemographic Characteristics of Participants
Research Priorities Identified
Satisfaction With Public Meeting
All respondents were satisfied with the meeting except 1, and all were satisfied with the length of the meeting except 2. All but 1 stated that they would attend a future public meeting to learn more about research.
A total of 17 caregivers returned the survey. All said they were satisfied with the meeting; most (n=14) said they would definitely and 3 would possibly attend future meetings on research.
Findings From Focus Groups Discussions
A total of 27 OAWCs and 17 caregivers participated in 1 of the 7 focus groups (Table 1), from which 3 themes emerged (Table 3): (1) motivation to be on a research team; (2) ability to make meaningful contributions; and (3) logistics required to facilitate engagement. Quotes from OAWCs and caregivers are provided in supplemental eTable 1.
Motivation to Be on a Team: Fewer than half of the OAWCs had participated in any type of study; caregivers had even less exposure to studies. Despite the limited exposure to research but based on their experiences as OAWCs and in the cancer treatment environment, most were very motivated to be on a team to improve care. Most OAWCs and caregivers had never been invited to participate in research. Several indicated that they felt they were not invited to participate in research because they perceived that older adults in Canadian society were not valued, even though they believed older adults could contribute very valuable insights based on their experiences. Some recalled having actively looked for clinical trials, which they saw as valuable for future treatments, but being told they were not eligible to participate. Many OAWCs indicated they did not know how to find clinical trials. Although some said that their physician encouraged them to participate in research studies, others commented that the physician clearance to participation required by some studies was a barrier because it was often difficult to obtain. Participants suggested that all patients (based on characteristics in their electronic medical record) should be automatically invited to participate in a study if they meet the criteria. Lastly, those who had been involved in research wanted to hear the final results of the study, yet most had never received that information from the study team. Almost all OAWCs and caregivers were willing to become team members.
Ability to Make Meaningful Contributions: Few OAWCs and their caregivers had ever heard of the term patient engagement in research, yet most said they would be willing to become a research team member if their voices and contributions could benefit them or future patients/caregivers. They had the time to be involved and said they would want to know in advance the objectives of the project and each meeting. They were willing to be involved for longer periods, although they preferred meeting once monthly or more frequently but for less time. Several OAWCs preferred to work in smaller groups, and preferred having more than 1 OAWC on the team so that they could connect with their peers during the project. Furthermore, having more than 1 OAWC on the team would ensure that continuity of the patient's voice was guaranteed. Notably, some OAWCs pointed out that a potential harm of engaging in research would be the possibility of learning that the prognosis and treatment options of their own disease were not as optimistic as previously believed.
Logistics Required to Facilitate Engagement Amidst Patient Preferences and Healthcare Status: OAWCs and their caregivers raised several logistical issues that needed to be addressed in order to facilitate engagement. Meeting flexibility (ie, day of the week) was important, as were length of the meeting (preferably no more than half a day), timing (not during rush hour and not after dark), providing transportation to those who need it, and accounting for winter conditions. OAWCs and caregivers preferred face-to-face meetings over telephone conferences/Skype
Findings From Focus Groups
OAWCs and caregivers felt that being trained to be a team member (eg, on research conduct and terminology) was important, but that training should be broken up into smaller sessions to facilitate retention of information. They also preferred receiving written training materials before team meetings and having access to a dedicated research team member who could offer a separate question and answer session before meetings. They commented that researchers should provide “translation for scientific articles and a glossary for terminologies.” Most participants agreed that it would be a “learn as you go” process, which was preferred over classes and courses in advance of the project.
Discussion
Our findings show that OAWCs are very interested in participating in studies, especially if they believe it would help them or future patients. Approximately half of the attendees at the public meetings had never been invited to participate in any studies, illustrating older adults' lack of accessibility to research. Although Townsley et al21 found that OAWCs do not seem to actively seek out clinical trials, some in our study said that they had done so but had been told that they were ineligible, whereas others did not know where to look. Designing protocols with less restrictive inclusion criteria can help increase older adults' access to studies.5 Increased involvement of older adults in the research process itself can help democratize the research process, increase accessibility, and enable their voices to be heard.12,13
A recent realist synthesis by McNeil et al22 developed a 5-stage engagement framework that can be used to enhance engagement. The 5 stages include environment, plan, establish, build, and transition. The environment stage refers to opportunities, or lack thereof, to engage patients and the accessibility issues needed for success, clearly discussed by our participants. The plan stage refers to the investigators planning for engagement; our participants clearly described the logistics that need to be taken into account. The establish stage refers to relationship-building among team members, which links back to the social aspects of being on a team—also clearly described by our participants. The build stage refers to the commitment over time, and the transition stage refers to the end of the research project; our participants clearly indicated they wanted to receive the findings of the projects in which they were engaged. Our findings thus align with this framework22 and provide a more detailed insight for engaging OAWCs and their caregivers.
In this study, the top research priorities identified included finding a cure, examining benefits/harms of complementary and alternative medicine for OAWCs, and improving communication. In Australia, the Cancer Council NSW partnered with Cancer Voices NSW to work with cancer consumers through workshops to set the research agenda for cancer care.23 These workshops included 32 participants ranging in age from 18 to 72 years, and top priorities included exploring how to diagnose cancer earlier (before metastatic disease), the extent to which palliative care guidelines are used, nutrition and lifestyle risk factors for cancer, how to address chemotherapy side effects, how to increase cancer screening rates, and what support is needed to help those affected return to normal activities. Some of the priorities align with our identified priorities but some do not, such as cancer screening and use of palliative care guidelines.23 This may be due to differences in age of participants (our participants were older and thus some were no longer eligible for the cancer population–based screening programs in Ontario, Canada). Improving communication and finding a cure for cancer were consistently identified as research priorities across all public meetings and focus groups. In a survey study of similar research priorities at The Royal Marsden Hospital, Moorcraft et al24 reported that the priorities varied by age, with younger patients rating early detection of recurrence and palliative treatment higher, and older adults rating side effect management as more important; these were not mentioned by our subjects.
A common challenge cited by researchers in patient engagement studies is logistics of engaging patients, such as funding and time.8 In our study, we arranged or compensated for transportation and were able to complete each session on time. Given the importance of engaging patients in research, it is imperative that more funding be allocated for patient engagement initiatives in order to fully support the efforts to actively involve these important partners in research.
Although our findings may not be generalizable, they do provide greater understanding of the importance of including OAWCs on teams, and their training needs to optimize their engagement. Our study included a small sample of OAWCs; it was an exploratory study using qualitative data collection. However, data saturation was obtained for the focus groups. Another limitation was our recruitment of older adults through flyers and newspaper ads. In fact, more than half of the study participants were not currently receiving any cancer treatment. However, these cancer survivors are the most likely to participate in research teams, because many of our OAWCs indicated that they would not have considered participating during their treatments.
Lastly, we did not specify which type of study when discussing OAWC participation on a research team. The study topic would impact their willingness, but because this was a first exploratory study, we chose a broad (any site/stage/treatment) rather than deep (specific site/stage/treatment) approach. Future studies should explore the willingness of older adults to participate on research teams in a larger, more diverse sample as well as explore more in-depth willingness and support needs for different types of studies (eg, clinical trials vs observational studies) and for different clinical groups (eg, early vs late stage, curative vs palliative treatment intent).
Conclusions
Overall, OAWCs are keen to participate in research and to be research team members, yet they are often not invited. Concerted efforts are needed to increase older adults' access to study participation and opportunities to be included in research teams.17,25,26 The social aspect of having older adults as part of a research team is important to take into consideration in future endeavors.
Despite the push for increasing engagement of patients and knowledge users, and despite there being a variety of patient engagement theories, frameworks, and models, the best methods for engagement have not been identified, and the impact of engagement on patients and caregivers is not fully understood.8,11,12,15,22 Although many studies have examined engagement, most have used qualitative methods, and there is currently no quantitative measurement tool that measures the impact of the engagement on study outcomes. Such a tool is clearly needed, and future similar studies should include one so that different methods of engagement can be compared to develop best practices.
Acknowledgments
We would like to thank all participants, volunteers, and partners who provided their support for this study: University Health Network, Mount Sinai Hospital, The Scarborough Hospital, St. Michael's Hospital, St. Joseph's Health Centre, Toronto East General Hospital, Sunnybrook Health Sciences Centre, Stronach Regional Cancer Centre, Cancer Care Ontario, The Leukemia & Lymphoma Society of Canada, Prostate Cancer Canada, Colorectal Cancer Association of Canada, Melanoma Network of Canada, Brain Tumour Foundation of Canada, Lung Cancer Canada, Kidney Cancer Canada, Canadian Cancer Survivor Network, Patients for Patient Safety Canada, CARP (national office and local chapters in Scarborough and Mississauga), Regional Geriatric Program of Toronto, and ELLICSR Health, Wellness & Cancer Survivorship Centre.
Dr. Hsu has disclosed that she has served on an advisory board for Pfizer and Celgene (unrelated to this project). The remaining authors have disclosed that they have no financial interests, arrangements, affiliations, or commercial interests with the manufacturers of any products discussed in this article or their competitors.
Dr. Puts is supported by a Canadian Institutes of Health Research New Investigator Award. Funding for this study was provided by Canadian Institutes of Health Research program: SPOR Patient Engagement – Collaboration (grant number 344008), and St. Michael's Hospital, University Health Network, Odette Cancer Centre, Leukemia & Lymphoma Society Canada, and Prostate Cancer Canada.
A poster presentation was presented at the International Society of Geriatric Oncology 2016 Annual Conference; November 17–19, 2016; Milan, Italy and the annual meeting of the MASCC/ISOO 2016 Annual Meeting on Supportive Care in Cancer; June 23–25, 2016; Adelaide, Australia. An oral presentation was given at the International Society of Geriatric Oncology 2015 Annual Conference; November 12–14, 2015; Prague, Czech Republic.
See JNCCN.org for supplemental online content.
References
- 1.↑
Scher KS, Hurria A. Under-representation of older adults in cancer registration trials: known problem, little progress. J Clin Oncol 2012;30:2036–2038.
- 2.
Talarico L, Chen G, Pazdur R. Enrollment of elderly patients in clinical trials for cancer drug registration: a 7-year experience by the US Food and Drug Administration. J Clin Oncol 2004;22:4626–4631.
- 3.
Yee KW, Pater JL, Pho L et al.. Enrollment of older patients in cancer treatment trials in Canada: why is age a barrier? J Clin Oncol 2003;21:1618–1623.
- 4.
Al-Refaie WB, Vickers SM, Zhong W et al.. Cancer trials versus the real world in the United States. Ann Surg 2011;254:438–442.
- 5.↑
Hurria A, Levit LA, Dale W et al.. Improving the evidence base for treating older adults with cancer: American Society of Clinical Oncology statement. J Clin Oncol 2015;33:3826–3833.
- 6.
Al-Refaie WB, Weinberg A, Nelson H. Are older adults adequately represented in surgical oncology trials? Bull Am Coll Surg 2013;98:52–53.
- 7.↑
Witham MD, George J. Clinical trial design for older people—time for a rethink. QJM 2014;107:15–16.
- 8.↑
Domecq JP, Prutsky G, Elraiyah T et al.. Patient engagement in research: a systematic review. BMC Health Serv Res 2014;14:89.
- 9.
Woolf SH, Zimmerman E, Haley A, Krist AH. Authentic engagement of patients and communities can transform research, practice, and policy. Health Aff (Millwood) 2016;35:590–594.
- 10.
Dudley L, Gamble C, Preston J et al.. What difference does patient and public involvement make and what are its pathways to impact? Qualitative study of patients and researchers from a cohort of randomised clinical trials. PLoS One 2015;10:e0128817.
- 11.↑
Carman KL, Workman TA. Engaging patients and consumers in research evidence: applying the conceptual model of patient and family engagement. Patient Educ Couns 2017;100:25–29.
- 12.↑
Smith SK, Selig W, Harker M et al.. Patient engagement practices in clinical research among patient groups, industry, and academia in the United States: a survey. PLoS One 2015;10:e0140232.
- 13.↑
Strategy for Patient-Oriented Research—Patient Engagement Framework. Canadian Institutes of Health Research Web stie. Available at: http://www.cihr-irsc.gc.ca/e/48413.html. Accessed August 21, 2017.
- 14.↑
Welcome to INVOLVE. INVOLVE Web site. Available at: http://www.invo.org.uk/. Accessed August 21, 2017.
- 15.↑
Forsythe LP, Ellis LE, Edmundson L et al.. Patient and stakeholder engagement in the PCORI pilot projects: description and lessons learned. J Gen Intern Med 2016;31:13–21.
- 16.↑
PCORI (Patient-Centered Outcomes Research Institute). Engagement Rubric for Applicants. Available at: https://www.pcori.org/sites/default/files/Engagement-Rubric.pdf. Accessed August 21, 2017.
- 17.↑
Brett J, Staniszewska S, Mockford C et al.. A systematic review of the impact of patient and public involvement on service users, researchers and communities. Patient 2014;7:387–395.
- 18.↑
Graneheim UH, Lundman B. Qualitative content analysis in nursing research: concepts, procedures and measures to achieve trustworthiness. Nurse Educ Today 2004;24:105–112.
- 19.
Hsieh HF, Shannon SE. Three approaches to qualitative content analysis. Qual Health Res 2005;15:1277–1288.
- 21.↑
Townsley CA, Chan KK, Pond GR et al.. Understanding the attitudes of the elderly towards enrolment into cancer clinical trials. BMC Cancer 2006;6:34.
- 22.↑
McNeil H, Elliott J, Huson K et al.. Engaging older adults in health care research and planning: a realist synthesis. Res Involve Engagem 2016;2:10.
- 23.↑
Saunders C, Crossing S. Towards meeting the research needs of Australian cancer consumers. BMC Res Notes 2012;5:667.
- 24.↑
Moorcraft SY, Sangha A, Peckitt C et al.. Does cancer research focus on areas of importance to patients? Ecancermedicalscience 2016;10:ed51.
- 25.↑
Hurria A, Mohile SG, Dale W. Research priorities in geriatric oncology: addressing the needs of an aging population. J Natl Compr Canc Netw 2012;10:286–288.
- 26.↑
Hurria A, Cohen HJ, Extermann M. Geriatric oncology research in the cooperative groups: a report of a SIOG special meeting. J Geriatr Oncol 2010;1:40–44.
