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Enrolling Older Adults Onto National Cancer Institute–Funded Clinical Trials in Community Oncology Clinics: Barriers and Solutions

Enrolling Older Adults Onto National Cancer Institute–Funded Clinical Trials in Community... In April 2021, the National Cancer Institute (NCI) Division of Cancer Prevention collaborated with the NCI Division of Cancer Treatment and Diagnosis to produce a virtual workshop that developed recommendations for enhancing NCI-sponsored clin- ical trial accrual of older adults. Prior to the workshop, a multidisciplinary group of stakeholders (eg, community oncologists, advanced practice practitioners, clinic and research staff, and patient advocates) gathered information related to accrual of older adults to clinical trials from the literature. Subsequently, a survey was conducted to detail NCI Community Oncology Research Program members’ perspective on accrual barriers for this population; 305 individuals responded to the survey. Barriers to clinical trial accruals included comorbidity-attributed trial ineligibility, transportation and time issues, concern that the proposed regimen is too toxic for older adults, patient or family caregiver declined participation, and lack of trials rel- evant to older patients. Identified solutions included broadening clinical trial inclusion criteria, increasing the number of clin- ical trials specifically designed for older adults, simplifying consent forms, improving recruitment materials for older adults and their families, and facilitating transportation vouchers. At the workshop, participants, including stakeholders, used prior literature and survey results to develop recommendations, including interventions to address clinician bias, implement geri- atric assessment, and promote clinician and staff engagement as mechanisms to improve accrual of older adults to clinical trials. Cancer diagnoses occur in 42% of patients aged 70 years and patients with cancer remain, especially for those who are aged older (1), yet less than 10% of patients in this age group partici- 70 years and older and who have aging-related conditions. In pate in National Cancer Institute (NCI) clinical trials (2). April 2021, the NCI Division of Cancer Prevention collaborated Consequently, care innovations established by clinical trials with the NCI Division of Cancer Treatment and Diagnosis to often lack efficacy and effectiveness in this older population. produce a virtual workshop that developed recommendations Gaps in knowledge on how to improve outcomes of older for enhancing NCI-sponsored clinical trial accrual of older Received: May 23, 2022; Revised: July 27, 2022; Accepted: August 19, 2022 Published by Oxford University Press 2022. This work is written by (a) US Government employee(s) and is in the public domain in the US. 117 Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 118 | J Natl Cancer Inst Monogr, 2022, Vol. 2022, No. 60 adults. A primary goal of the workshop was to identify modifi- a list of available protocols, e-mail and mail reminders, and a able barriers to clinical trial participation among older patients, case discussion seminar); the study’s primary endpoint was including clinician bias. Prior to the workshop, a multidiscipli- percentage of older adults accrued to phase II and III trials. nary group of researchers, NCI staff, and stakeholders (eg, com- Analyses did not reveal any accrual differences between the 2 munity oncologists, advanced practice practitioners [APP], clinic groups. The investigators concluded that more intense and and research staff, and patient advocates) convened monthly multifaceted approaches may be necessary to increase accrual. for 6 months. The group collated evidence from the literature There are no other published randomized controlled trials prior to the workshop, and qualitative themes from the litera- explicitly striving to increase accrual of older adults to clinical ture guided the development of a survey to assess NCI trials (1). Community Oncology Research Program (NCORP) members’ More recent studies affirm that accrual challenges persist. perspective on accrual barriers of older adults to NCI-funded Freedman and colleagues’ (9) investigation of accrual barriers cancer clinical trials in community oncology clinics. NCORP is a noted that respondents (clinicians enrolling patients onto stud- national network that brings cancer clinical trials and cancer ies for the Alliance Cooperative Group) most frequently identi- care delivery studies to patients where they live in their com- fied the following barriers: inability to meet eligibility criteria munities; NCORP sites are community oncology practices, and (67.5%), treatment regimens were too toxic (44.4%), transporta- the network includes more than 9000 physicians, APPs, nurses, tion issues (44%), patient or family preference not to enroll and research staff (3). The survey primarily solicited community (35%), and concern for limited life expectancy in older patients oncology clinicians and their research staff because community (28%). Potential recommended strategies included dedicated tri- oncology clinics provide care for the majority of older patients als for older adults (36.3%), minimizing exclusion criteria focus- with cancer (4). At the workshop, participants reviewed the lit- ing on comorbidity (35.5%), developing specific strategies for erature synthesis and survey results and discussed pragmatic those aged 65 years and older separated from those aged 70 recommendations that could guide NCI efforts to improve years or older (33.2%), requiring expansion cohorts of older accrual of older adults to cancer clinical trials. Workshop partic- patients (30%) and creating standardized educational interven- ipants included the multidisciplinary group that convened prior tions for family members and caregivers (22.3%). to the meeting; additional National Institutes of Health staff Sedrak et al. (1) published the most comprehensive system- and scientific leaders, leaders of the NCI-funded cooperative atic review of barriers and interventions for older adult partici- groups, and stakeholders also attended the workshop. pation in clinical trials to date. Investigators employed PRISMA In this manuscript, investigators report the literature that guidelines (10) to identify 145 full-text articles for review. was considered to inform the workshop agenda and activities. Investigators subsequently included only 13 studies that identi- Survey results detailing NCORP members’ perspective on fied systemic, provider, patient, and caregiver barriers in the accrual barriers for this population and potential solutions are analysis. Systemic barriers included eligibility criteria, consent also included. The referenced literature and survey results form language, and trial availability. Provider barriers included informed pragmatic recommendations to address common toxicity concerns, preference for other treatments, time and oncology team–identified barriers to accrual of older adults to burden to enroll on a clinical trial, lack of personnel, preference NCI-funded cancer clinical trials. against research, and lack of awareness of eligible trials. Patient barriers included knowledge of clinical trials, transportation, time and burden, toxicity concerns, financial concerns, belief that they were too old, and emotional burdens. Caregiver con- Overview of Key Manuscripts From the cerns included burden and preference against research. Literature Recommendations to expand inclusion of older adults to cancer Tejeda and colleagues (5) reported age disparities in NCI- clinical trials included specific trial design for older adults, sponsored cancer treatment trials as early as the 1980s. Trimble measurement of relevant endpoints, broadening of eligibility et al. (6) later noted older adults were underrepresented in clini- criteria, addressing specific site and stakeholder barriers, prag- cal trials, particularly in trials studying the safety and efficacy matic clinical trial design, and leverage of real-world data. of treatment for cancers disproportionately impacting this pop- More recent reports affirm accrual barriers’ persistence, with ulation; prostate cancer, predominantly observed among older the current pandemic exacerbating preexisting roadblocks men, provided the exception. Kornblith and colleagues’ pilot (11,12). Consequently, investigators surveyed community oncol- study (7) assessed provider-perceived accrual barriers to breast ogy clinicians and staff within NCORP to clarify current percep- cancer clinical trials. Respondents in this pilot study (n¼ 156; tions and solicit recommendations to address barriers in this 85% oncologists) noted that transportation needs (68%), comor- current climate. bid conditions (53%), treatment toxicities (51%), poor compli- ance due to difficulty understanding complicated trials (50%), and patient ineligibility per study inclusion criteria (36%) pre- NCORP Survey sented accrual challenges for older adults. Proposed solutions suggested by the respondents included dedicated clinic person- Methods nel to explain clinical trials to older patients (69%), dedicated educational material for older adults (63%), provision of trans- The aforementioned studies informed NCORP survey questions portation (63%), better educational material for family members to assess respondent perceptions about barriers and solutions (59%), and fewer exclusion criteria (49%). and use a Likert scale of 0-5 (0 ¼ never or the least; 5 ¼ always Kimmick et al. (8) designed and tested a geriatric educational or the most). The multidisciplinary group adapted survey ques- intervention to improve cooperative group–sponsored treat- tions from previously completed studies for this study (7,9). ment trial accrual of cancer patients aged 65 years and older. Investigators invited participants to rank their top 5 barriers Institutions received standard information (n¼ 73) or an educa- and solutions and to comment on their own experience or per- tional intervention (educational seminar, educational materials, spective on the noted barriers in open-ended questions, Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 J. O. Hopkins et al. |119 including possible solutions and research gaps. Investigators trial, and ability to comply. Many respondents reported family solicited all NCORP clinicians (physicians, APPs, nurses) and members needed to be more involved in trial design owing to staff (including coordinators and administrators) and collected their presumed knowledge of the patient or challenges patients data anonymously via a web-based platform. The University of face; care navigators also are of great importance to facilitate Rochester NCORP Research Base received and analyzed the de- patient involvement and overcome barriers. identified data in aggregate. To develop qualitative themes, a The top 5 rated solutions were as follows: broadening clini- thematic analysis approach (13) was used, which included 1) cal trial inclusion criteria (75% rated in the top 5); increasing the quotes from the open-ended questions were pulled from the number of clinical trials specifically designed for older adults database into an excel document in a tabular form; 2) using (70%); simplifying consent forms (56%); improving recruitment inductive open-coding, 2 reviewers (KM and SG) organized materials for older adults and their families (52%); and facilitat- themes into similar categories; 3) themes were reviewed by the ing transportation vouchers (52%). Table 2 reports mean scores authors; and 4) exemplar quotes were identified for themes by for solutions and exemplar quotes. the authors. An important theme from the open-ended questions cen- tered on technological barriers. Specifically, providers reported data collection concerns (patient-reported outcomes or virtual Results visits) requiring an app, smartphone, or internet access may limit accrual of older adults. Respondents advocated research- Respondent Characteristics ers retaining traditional data collection media (eg, paper and A total of 305 individuals responded to the survey; 50% were pencil, with one respondent stating, “ditch the electronic coordinators, 38% were physicians, 5% were administrators, 3% requirements”) (Table 3). were APPs, and 5% categorized themselves as other. Of the physicians, 13% self-identified as medical oncologists, 12% as an NCORP principal investigators, 6% as an NCORP physician, 4% as a surgeon, and 3% as a radiation oncologist. Seventy- Discussion three percent identified as female. Of the individuals, 76% The review of the literature and the NCORP survey results high- reported age as between 36 and 65 years, 14% were aged light important barriers to clinical trial accrual for older adults younger than 26 years, and 9% were aged older than 65 years. A with cancer in community oncology clinics. Although several of total of 58% reported being in practice for 11 or more years, and these barriers were reported in previous studies focused on 20% identified as members of a community cancer center, 37% accrual of older adults in academic cancer centers, it is impor- identified as being in private practice, and 37% worked in aca- tant to understand the impact of the barriers in community demic medical centers. Of the respondents, 33% characterized oncology clinics where most older adults are cared for. A quali- their practices as 26% to 50% rural, 43% had less than 25% rural tative analysis of medical oncologists (24 academic and 20 from patients, 6% of practices were 76% to 100% rural, and 6% were the community) previously demonstrated differences in per- not rural. ceived barriers; community oncologists were more likely to report that patient understanding and caregiver burden Barriers and Solutions impacted accrual than academic oncologists (14). Given the The top 5 barriers to accrual included comorbidity-attributed increasing focus on electronic methods of data capture and clin- trial ineligibility (84% chose as a top 5 barrier); transportation ical service delivery, an important theme that emerged from issues and the time involved with clinical trial participation this analysis was difficulties with having older adults complete (58%), concern that the proposed regimen is too toxic for older electronic requirements for clinical trial data capture. As these adults (56%), patient or family caregiver declined participation requirements grow in an effort to increase access to trials and (49%), and lack of trials relevant to adult patients (42%). These manage pandemic-related concerns with coming into the office, barriers also had the highest mean scores on the Likert scale for an unintentional and potentially adverse outcome could be a concern (Table 1). Barriers rated relatively less problematic further disparity in accrual of older adults from community included fear of patient compliance, the time required to dis- oncology clinics to cancer clinical trials. cuss or explain a clinical trial to an older adult, physician bias, Eligibility restrictions in protocols are a long-standing barrier requirement for some trials to perform geriatric assessment to accrual of older adults in clinical trials. NCORP survey (GA), and lack of knowledge to assess fitness prior to respondents listed broadening eligibility as the top solution for enrollment. accrual. In one national study of 5499 patients, investigators Qualitative themes regarding barriers included eligibility found that having 1 or more comorbidities was associated with concerns, perceptions that older patients choose less toxic fewer trial discussions and correspondingly less trial participa- treatments than proposed in the clinical trial and want trial tion (15). The American Society of Clinical Oncology and the designs for them specifically (vs accrual onto trials open to any- Friends of Cancer Research have published robust guidelines on one who meets eligibility), impressions that clinical trials are how to develop studies to broaden eligibility with regard to too burdensome for older adults, and concerns that there is not comorbidity, prior therapies, concomitant medications, and sufficient family and caregiver support (Table 1). Clinicians and performance status (16-19). By following this guidance, it is pro- staff reported believing most supportive care trials are too bur- jected that accrual of older adults to clinical trials would densome for older patients and doctors and nurses act as gate- increase (15). Further, guidelines included a recommendation to keepers. Respondents expressed concern over technology include a more optimal functional status evaluation (such as expectations (eg, smartphone availability) and presumed pro- instrumental activities of daily living) when assessing perform- spective enrollees desire paper option for questionnaires. ance status. A robust evidence base indicates oncologists bene- Respondents also expressed that family and caregivers are fit from objective tools to assess the performance status and essential and should be included in the research process as fitness of older adults accurately (20). Clinicians may assume fit much as possible to support patient’s well-being, adherence to older adults are at high risk of adverse outcomes because of Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 120 | J Natl Cancer Inst Monogr, 2022, Vol. 2022, No. 60 Table 1. Barriers with most concern Barrier with most concern Mean (SD) Median (IQR) Range Exemplar quotes Failure to meet clinical trial eligibility require- 3.34 (0.70) 3 (1) 1-5 • “Organ function eligibility requirements may ments because of comorbidities be too strict for older adults eg, creatinine clearance.” • “The single biggest barrier is creatinine clear- ance. I would say that 90% of my patients older than 75 cannot meet the creatinine clearance threshold specified for any study.” • “I have a lot of older adults fail because the lab entry criteria are too strict and they are often mildly anemic and in real life I would treat but would not be allowed in trials.” • “Comorbidities and specifically previous can- cers have been a big issue.” Transportation issues; distance to the treatment 3.09 (0.89) 3 (2) 1-5 • “Lack of payment for hotel and transportation center, time considerations for our rural patients.” • “VA insurance.” • “Lack of CRA support at remote part time rural clinic sites.” • “Time commitment related to a study can be a huge barrier for older adults. They would rather have to spend less time in my setting (hospital).” • “Enrollment takes too long.” Proposed regimen is too toxic for the older adults 3.03 (0.81) 3 (0.75) 1-5 • “In some instances, patients themselves opt for less toxic approaches due to age, performance status, quality of life concerns, and perceived life expectancy.” • “In elderly or patients with many comorbid- ities, they are either ineligible or not suitable for aggressive chemotherapy regimens.” • “Hearing loss is a major barrier to trial enroll- ment in the elderly.” • “Concerns about cognitive capacity for consent.” Patient or family and caregiver preferences not to 2.87 (0.92) 3 (2) 1-5 • “Older patients are choosing not to treat their participate in clinical research cancer.” • “Patients feeling too overwhelmed at new diagnosis.” Lack of trials relevant to older adult patients 2.85 (1.05) 3 (2) 1-5 • “Docs and nurses and clinical staff frequently think supportive care trials are too burdensome for elderly patients and the clinical staff act as barriers and gatekeepers.” patients who are more vulnerable and frailer. A recent system- chronologic age alone. Moreover, many providers mislabel aging-related conditions in older patients who are frailer, lead- atic review demonstrated that one of the most frequent reasons ing to undertreatment of fit older adults and overtreatment of for GA inclusion in clinical trials was the ability to recruit study older adults (21). Clinicians can employ GA to minimize biased participants based on frailty level. Use of GA to evaluate frailty assessment and improve trials assessment and treatment pro- as part of trial eligibility will add information that is normally priety. GA, including shorter screening tools and abbreviated not captured as part of routine oncology performance status versions (20,22,23), provides 2 benefits. First, the GA encourages evaluations (24). GA information can be used to identify patients providers to utilize established, standardized metrics to assess who have characteristics that lead to adverse outcomes from recruitment propriety. Such metrics may refine or correct clini- treatment (2,20). With GA information, clinicians may more cian biases and minimize their influence on trial solicitation. readily, validly, and reliably discern study-eligible patients, Second, these standardized metrics can inform protocol revi- thereby allowing more time for clinicians to promote and dis- sions expanding or restricting eligibility. Evidence-based proto- cuss trials with those truly eligible, and may aid in retention of col revisions, encouraged by reliable and valid GA assessment, older adults to clinical trials (24-26). Workshop participants may increase solicitation frequency, even if revisions reduce advocated for integrating GA into cancer clinical trials to increase accrual of older adults who have patient characteristics the number of study-eligible patients for trials that are designed for fit patients. These data can guide alternative trials for that are more representative of older adults cared for in Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 J. O. Hopkins et al. |121 Table 2. Most supported solution Most supported solution Mean (SD) Median (IQR) Range Exemplar quotes Real-world exclusion criteria including the usual 4.10 (1.01) 4 (1) 1-5 • “Less stringent eligibility criteria related to comorbidities older adults have renal and liver function as well as comorbid- ities would also make it easier to enroll older adults.” • “Definitely need to expand criteria including ECOG to 0-2 or up to 3 if felt to be disease related; CKD and other common comorbidities permitted.” • “Number 1 would be to make inclusion exclu- sion criteria age friendly.” Create trials specifically for the older adults 4.01 (0.98) 4 (1) 1-5 • “Dosage and/or treatment options should be modified to include safer treatment options for elderly participants.” Simplify consent forms 3.79 (1.10) 4 (2) 1-5 • “Simplify things (the consent, provide tools to help patients and their families stay organized or better understand the trial and its activities).” Targeted trial recruitment material for older 3.71 (1.03) 4 (1) 1-5 • “Have a rundown created for each study, show- adults and their family/caregivers ing exactly what would be expected on the study from the patient’s point of view.” • “Support groups—identify other patients who can help ‘mentor’ particularly patients who are widowed and live alone.” • “Generic (not study-specific) research recruit- ment materials noting benefit to future generations.” Provide transportation voucher or gas card for 3.64 (1.13) 4 (2) 1-5 • “Assistance with insurance issues and co-pays trial participants 65 years and older for those on fixed budgets.” • “Transportation vouchers should be done for everyone.” • “Leverage home health, virtual medicine, or other vehicles to fulfill research requirements and data collection while minimizing patient expense, discomfort and burden on family/ support.” CKD ¼ chronic kidney disease; ECS ¼ Eastern Cooperative Oncology Group. community oncology clinics. As one example, a NCI-funded clinicians and staff noted that requiring internet for studies trial evaluating a GA intervention for reducing toxicity, con- would remain a barrier for older adults. There have been data ducted in the NCORP network, enrolled a high prevalence of supporting feasibility of remote (ie, telemedicine) visits for GA, older adults with comorbidities (27,28). These studies provide however, expanding trials into community oncology clinics so evidence that studies designed specifically for older adults that that patients have the ability to participate locally in person integrate GA can be successful and increase accrual of this remains a strong recommendation. Further, in the open-ended underrepresented population. Other manuscripts were devel- questions, NCORP clinicians and staff reported that they had oped by workshop participants for this supplement review opti- concerns with the ability of older adults to complete electronic mal study design for clinical trials and integration of GA into requirements for data reporting, especially patient-reported these trials. outcomes and quality-of-life questionnaires. Several com- The pandemic has increased concerns about the access of mented that offering paper-and-pencil approaches is needed vulnerable groups to clinical trials. There were negative conse- for older adults. Although there is data to support feasibility of quences to oncology clinical trial participation that led to con- remote collection of data for older adults (31), the NCORP survey sideration of the use of technology solutions in an attempt to participant recommendations to “continue to offer QOLs, tutori- maintain equitable participation (29). The NCORP survey dem- als, and other patient materials in paper form vs just electronic” onstrated that transportation issues (because of travel time and should be heeded. Trials should be designed with pragmatic distance as well as need for caregiver support) remain a serious design elements and components, offering flexibility and choice barrier. In another study, a survey of 1183 patients with cancer whenever possible so older patients can choose where they demonstrated that although the majority indicated they would wish to participate and how they wish to provide information. be more likely to participate in a trial if remote technology was Engaging patient and caregivers as research partners when included, older adults were more likely to say they would partic- developing study procedures can foster feasibility with technol- ipate in trials only if they were closer to home (30). NCORP ogy options (32). Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 122 | J Natl Cancer Inst Monogr, 2022, Vol. 2022, No. 60 Table 3. Technology barriers and solutions Barriers Solutions • “Use of technology to collect data (ePRO or virtual visit).” • “Avoid electronic diaries, PROs, etc.” • “Trials require ‘extra work’ that may be considered burdensome or • “Provide nontech options for questionnaires, ie, paper forms com- overwhelming to the elderly, including the use of electronic pleted at clinic visit.” patient reported outcome devices.” • “While technology is great, continue to offer QOLs, tutorials, and • “Having required tech/internet access for needed QOLs.” other patient materials in paper form vs just electronic.” • “Having to use ePRO’s or an app.” • “Please stop creating protocols that require older patients to have • “Study requires patient to use technology, ie, smartphone apps, and be facile with internet participation and other electronic computer-generated questionnaires, video conferencing.” ideas.” • “Many elderly are not willing to do electronic questionnaires or • “Offer PROs on paper as opposed to electronically.” study requirements on an app or smartphone, but much prefer • “Ditch the electronic requirements.” paper forms completed during an office visit.” • “Also, many older adults do not have electronics or do not have the technical skill level to complete study activities online.” ePRO ¼ electronic patient-reported outcome; QOL ¼ quality of life. In addition to reviewing and discussing the survey results, provide a context in which explicit benevolence may mediate the workshop provided a forum for participants to discuss addi- trial recruitment and accrual. tional accrual barriers, notably implicit or unintentional bias, In circumstances where there is limited evidence for safety and explored strategies that may mitigate this presumed clini- and efficacy, clinicians may more readily rely on clinical experi- ence when considering accrual of older adults to clinical trials. cal trial barrier. Workshop participants additionally discussed how engagement of clinical staff could improve clinical trial Clinicians relying on erroneous estimates may demonstrate an accrual of older adults. “insensitivity to prior probability of outcomes” (41). Specifically, clinicians potentially evaluate the likelihood a patient is study eligible or ineligible referencing the degree to which the patient exhibits an exclusion criterion–relevant stereotype. For exam- Bias Related to Accrual of Older Adults to Clinical Trials ple, clinicians may unconsciously label all or most older adults Bias is a stereotype that leads to a distorted judgment nega- as frail because the majority of their frail patients are older. tively impacting an already disadvantaged group (33-36). This insensitivity potentially begets the “explicit[ly] benevolent” Aspects of clinician bias may reflect well-intended aspirations stance, “I believe older adult patients are frail. I aspire to do no designed to protect or advance disadvantaged groups. Results harm and protect my patients. Therefore, I will not subject my from the survey support that respondents believe that clinicians older adult patients to [a given] clinical trial and decline to and staff act as gatekeepers for trial enrollment. This “explicit recruit this patient.” Although clinicians intend to do no harm, benevolence” may reinforce the very disparity well-intended these beliefs stem from age-related stereotypes (ie, ageism) that perpetuate inequities (35,42). Addressing this perspective is a clinicians aspire to mitigate. For older adults, explicit benevo- lence manifests during the assessment of patients’ trial eligibil- prerequisite to trial design innovation. Indeed, pragmatic trials ity (a clinician-level consideration). Clinicians intend to first, do may hold promise for increasing accessibility, assuaging no harm. Where uncertain about trial propriety (ie, patient fit- resource use, and imposing less patient burden (43). However, ness and/or concerns about toxicity), clinicians may err toward study design and inclusion criteria pragmatism, though neces- exclusion, not solicitation. Further, clinicians align both patient sary, may still fail to address the clinician’s interpretation of the care and trial accrual principles on tenets of justice, benefi- inclusion criteria. Consequently, clinicians may employ well- cence, and respect for persons. When contemplating trial meaning, but flawed, exclusionary defaults, regardless of a recruitment, clinicians consider whether a trial advances or study (or inclusion criteria’s) pragmatic qualities. deprives a patient of care that the provider deems essential or Addressing explicit benevolence and/or bias is challenging. Systemic modifications to clinical trials, including expansion of asks patients to undergo increased burden (justice). Clinicians commit to securing patients’ well-being, which includes maxi- inclusion criteria, will not produce change unless individual mizing benefit and minimizing harm (beneficence). Finally, clinicians acknowledge inherent biases and, once recognized, clinicians aspire to affirm patients’ autonomy and to protect change behavior. By reflecting on biases, clinicians can critically examine their own opinion of a study’s capacity to advance those less positioned to act independently (respect for persons). These aspirational classifications potentially motivate an clinical practice. Clinicians can constructively articulate their explicit benevolence that blunts trial solicitation and accrual. In concerns to investigative teams, including study sponsors and addition, the care encounter is fraught with competing the principal investigators (PIs). Likewise, study teams can demands and perceptions that mitigate trial engagement actively engage community oncology stakeholders to co- (1,37,38). Those particularly germane to trial accrual include develop trials prioritizing older adult recruitment. Apart from provider belief that their organization does not value research sponsor and PI education, these discussions also encourage enough to credit in career advancement considerations, lack of clinician and practice ownership, responsibility, and account- access to research training, perceived inability to influence ability for accrual effort. Such discussions potentially discour- practice through research, and belief that research teams age provider rationalization (eg, “This study is too difficult”) by identifying solutions early in trial development. Clinicians can underestimate the time required to execute research tasks (39,40). Thus, competing care demands and cultural barriers also communicate their opinions on a study’s value thereby Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 J. O. Hopkins et al. |123 directing sponsor and PI efforts from potentially futile protocol practices. Although the workshop discussed long-standing bar- amendments. Information gleaned from this transparency riers to accrual, we were able to identify solutions that could allows PIs to tailor studies, particularly recruitment, to practice facilitate accrual of older adults to NCI-funded clinical trials in and/or organization characteristics to improve recruitment. PIs community oncology clinics; this information will guide inter- can use this feedback to transition from patient-focused inclu- ventions and efforts led by the NCI to improve accrual of older sion criteria (eg, age, disease status) to multilevel inclusion cri- adults to clinical trials. Consequently, we encourage interven- teria that include matching studies to clinician and practice tions targeting patient, providers, families and caregivers, and resources, culture, and goals (40). Such an approach may restrict organizations in which care teams contemplate trial propriety. site availability but maximize recruitment at the sites electing Ultimately, stakeholders must also consider the community to participate. Multilevel research is needed to rigorously assess context and sociopolitical landscape that informs, reinforces, the merits of these potential approaches (44). and rewards organizational structures, policies, and activities that inherently impede accrual of older adults to NCI-funded cancer clinical trials. Clinician and Staff Engagement as a Mechanism to Increase Enrollment of Older Adults to Clinical Trials Funding The previous 20 years produced an explosion of APPs including This study received funding from the National Cancer nurse practitioners, physician’s assistants, and clinical pharma- Institute (UG1CA189961 for the URCC NCORP Research Base cists, who more directly participate in oncology patient care, and UG1CA189804 for the Hawaii Minority/Underserved including older adults. APPs report interest in increasing their NCORP) and the National Institute on Aging (K24AG056589, participation in clinical research and desire inclusion in clinical R33AG059206 to SGM). trials teams (45,46). Therefore, APPs may help address staffing- attributed accrual barriers. Additionally, APPs can facilitate edu- cation for older adults and caregivers, and this education may Notes better ensure informed decisions regarding clinical research participation. Role of the funder: The funder, the NIH, is a sponsor for the con- Clinicians express concern about extra time required to ference and for all the manuscripts in the Monograph. This enroll patients onto trials; however, they may mitigate this bar- manuscript is a collaboration between investigators and NIH rier by employing a team approach. For example, an oncologist employees. may introduce the study as part of the standard of care, and Disclosures: There are no disclosures to report for any of the then the APP subsequently educates the patient on the treat- authors. ment and describes the clinical trial option. For patients expressing interest, the APP can solicit the clinical research Author contributions: Conceptualization all; Funding acquisi- coordinator to more explicitly describe the trial to the patient tion DS; Data collection DS, SM; Project administration SM, MW; and family. This team approach can lessen accrual burden Data analysis SM, SG, KM, MW; Data interpretation all; Writing among team members and may allay the “time and burden to all except DS; Writing review all. enroll” (47). APPs and nurses also report routinely providing patient care coordination, follow-up visits, and toxicity checks as part of their daily practice for older patients with cancer (48). Data Availability Care teams typically include APPs and nurses particularly posi- tioned to address the identified barriers (eg, toxicity manage- Data (ie, survey responses) were collected by NIH and reported ment, visit coordination) (49). in aggregate. The University of Rochester NCI Community Forty years of research reveals suboptimal accrual of older Oncology Research Program Research Base analyzed the data. adults in clinical trials, with investigators identifying barriers No identifiers were collected. Raw aggregate data can be and proposing solutions. 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Oncol. 2021;12(7):1000-1004. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png JNCI Monographs Oxford University Press

Enrolling Older Adults Onto National Cancer Institute–Funded Clinical Trials in Community Oncology Clinics: Barriers and Solutions

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Abstract

In April 2021, the National Cancer Institute (NCI) Division of Cancer Prevention collaborated with the NCI Division of Cancer Treatment and Diagnosis to produce a virtual workshop that developed recommendations for enhancing NCI-sponsored clin- ical trial accrual of older adults. Prior to the workshop, a multidisciplinary group of stakeholders (eg, community oncologists, advanced practice practitioners, clinic and research staff, and patient advocates) gathered information related to accrual of older adults to clinical trials from the literature. Subsequently, a survey was conducted to detail NCI Community Oncology Research Program members’ perspective on accrual barriers for this population; 305 individuals responded to the survey. Barriers to clinical trial accruals included comorbidity-attributed trial ineligibility, transportation and time issues, concern that the proposed regimen is too toxic for older adults, patient or family caregiver declined participation, and lack of trials rel- evant to older patients. Identified solutions included broadening clinical trial inclusion criteria, increasing the number of clin- ical trials specifically designed for older adults, simplifying consent forms, improving recruitment materials for older adults and their families, and facilitating transportation vouchers. At the workshop, participants, including stakeholders, used prior literature and survey results to develop recommendations, including interventions to address clinician bias, implement geri- atric assessment, and promote clinician and staff engagement as mechanisms to improve accrual of older adults to clinical trials. Cancer diagnoses occur in 42% of patients aged 70 years and patients with cancer remain, especially for those who are aged older (1), yet less than 10% of patients in this age group partici- 70 years and older and who have aging-related conditions. In pate in National Cancer Institute (NCI) clinical trials (2). April 2021, the NCI Division of Cancer Prevention collaborated Consequently, care innovations established by clinical trials with the NCI Division of Cancer Treatment and Diagnosis to often lack efficacy and effectiveness in this older population. produce a virtual workshop that developed recommendations Gaps in knowledge on how to improve outcomes of older for enhancing NCI-sponsored clinical trial accrual of older Received: May 23, 2022; Revised: July 27, 2022; Accepted: August 19, 2022 Published by Oxford University Press 2022. This work is written by (a) US Government employee(s) and is in the public domain in the US. 117 Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 118 | J Natl Cancer Inst Monogr, 2022, Vol. 2022, No. 60 adults. A primary goal of the workshop was to identify modifi- a list of available protocols, e-mail and mail reminders, and a able barriers to clinical trial participation among older patients, case discussion seminar); the study’s primary endpoint was including clinician bias. Prior to the workshop, a multidiscipli- percentage of older adults accrued to phase II and III trials. nary group of researchers, NCI staff, and stakeholders (eg, com- Analyses did not reveal any accrual differences between the 2 munity oncologists, advanced practice practitioners [APP], clinic groups. The investigators concluded that more intense and and research staff, and patient advocates) convened monthly multifaceted approaches may be necessary to increase accrual. for 6 months. The group collated evidence from the literature There are no other published randomized controlled trials prior to the workshop, and qualitative themes from the litera- explicitly striving to increase accrual of older adults to clinical ture guided the development of a survey to assess NCI trials (1). Community Oncology Research Program (NCORP) members’ More recent studies affirm that accrual challenges persist. perspective on accrual barriers of older adults to NCI-funded Freedman and colleagues’ (9) investigation of accrual barriers cancer clinical trials in community oncology clinics. NCORP is a noted that respondents (clinicians enrolling patients onto stud- national network that brings cancer clinical trials and cancer ies for the Alliance Cooperative Group) most frequently identi- care delivery studies to patients where they live in their com- fied the following barriers: inability to meet eligibility criteria munities; NCORP sites are community oncology practices, and (67.5%), treatment regimens were too toxic (44.4%), transporta- the network includes more than 9000 physicians, APPs, nurses, tion issues (44%), patient or family preference not to enroll and research staff (3). The survey primarily solicited community (35%), and concern for limited life expectancy in older patients oncology clinicians and their research staff because community (28%). Potential recommended strategies included dedicated tri- oncology clinics provide care for the majority of older patients als for older adults (36.3%), minimizing exclusion criteria focus- with cancer (4). At the workshop, participants reviewed the lit- ing on comorbidity (35.5%), developing specific strategies for erature synthesis and survey results and discussed pragmatic those aged 65 years and older separated from those aged 70 recommendations that could guide NCI efforts to improve years or older (33.2%), requiring expansion cohorts of older accrual of older adults to cancer clinical trials. Workshop partic- patients (30%) and creating standardized educational interven- ipants included the multidisciplinary group that convened prior tions for family members and caregivers (22.3%). to the meeting; additional National Institutes of Health staff Sedrak et al. (1) published the most comprehensive system- and scientific leaders, leaders of the NCI-funded cooperative atic review of barriers and interventions for older adult partici- groups, and stakeholders also attended the workshop. pation in clinical trials to date. Investigators employed PRISMA In this manuscript, investigators report the literature that guidelines (10) to identify 145 full-text articles for review. was considered to inform the workshop agenda and activities. Investigators subsequently included only 13 studies that identi- Survey results detailing NCORP members’ perspective on fied systemic, provider, patient, and caregiver barriers in the accrual barriers for this population and potential solutions are analysis. Systemic barriers included eligibility criteria, consent also included. The referenced literature and survey results form language, and trial availability. Provider barriers included informed pragmatic recommendations to address common toxicity concerns, preference for other treatments, time and oncology team–identified barriers to accrual of older adults to burden to enroll on a clinical trial, lack of personnel, preference NCI-funded cancer clinical trials. against research, and lack of awareness of eligible trials. Patient barriers included knowledge of clinical trials, transportation, time and burden, toxicity concerns, financial concerns, belief that they were too old, and emotional burdens. Caregiver con- Overview of Key Manuscripts From the cerns included burden and preference against research. Literature Recommendations to expand inclusion of older adults to cancer Tejeda and colleagues (5) reported age disparities in NCI- clinical trials included specific trial design for older adults, sponsored cancer treatment trials as early as the 1980s. Trimble measurement of relevant endpoints, broadening of eligibility et al. (6) later noted older adults were underrepresented in clini- criteria, addressing specific site and stakeholder barriers, prag- cal trials, particularly in trials studying the safety and efficacy matic clinical trial design, and leverage of real-world data. of treatment for cancers disproportionately impacting this pop- More recent reports affirm accrual barriers’ persistence, with ulation; prostate cancer, predominantly observed among older the current pandemic exacerbating preexisting roadblocks men, provided the exception. Kornblith and colleagues’ pilot (11,12). Consequently, investigators surveyed community oncol- study (7) assessed provider-perceived accrual barriers to breast ogy clinicians and staff within NCORP to clarify current percep- cancer clinical trials. Respondents in this pilot study (n¼ 156; tions and solicit recommendations to address barriers in this 85% oncologists) noted that transportation needs (68%), comor- current climate. bid conditions (53%), treatment toxicities (51%), poor compli- ance due to difficulty understanding complicated trials (50%), and patient ineligibility per study inclusion criteria (36%) pre- NCORP Survey sented accrual challenges for older adults. Proposed solutions suggested by the respondents included dedicated clinic person- Methods nel to explain clinical trials to older patients (69%), dedicated educational material for older adults (63%), provision of trans- The aforementioned studies informed NCORP survey questions portation (63%), better educational material for family members to assess respondent perceptions about barriers and solutions (59%), and fewer exclusion criteria (49%). and use a Likert scale of 0-5 (0 ¼ never or the least; 5 ¼ always Kimmick et al. (8) designed and tested a geriatric educational or the most). The multidisciplinary group adapted survey ques- intervention to improve cooperative group–sponsored treat- tions from previously completed studies for this study (7,9). ment trial accrual of cancer patients aged 65 years and older. Investigators invited participants to rank their top 5 barriers Institutions received standard information (n¼ 73) or an educa- and solutions and to comment on their own experience or per- tional intervention (educational seminar, educational materials, spective on the noted barriers in open-ended questions, Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 J. O. Hopkins et al. |119 including possible solutions and research gaps. Investigators trial, and ability to comply. Many respondents reported family solicited all NCORP clinicians (physicians, APPs, nurses) and members needed to be more involved in trial design owing to staff (including coordinators and administrators) and collected their presumed knowledge of the patient or challenges patients data anonymously via a web-based platform. The University of face; care navigators also are of great importance to facilitate Rochester NCORP Research Base received and analyzed the de- patient involvement and overcome barriers. identified data in aggregate. To develop qualitative themes, a The top 5 rated solutions were as follows: broadening clini- thematic analysis approach (13) was used, which included 1) cal trial inclusion criteria (75% rated in the top 5); increasing the quotes from the open-ended questions were pulled from the number of clinical trials specifically designed for older adults database into an excel document in a tabular form; 2) using (70%); simplifying consent forms (56%); improving recruitment inductive open-coding, 2 reviewers (KM and SG) organized materials for older adults and their families (52%); and facilitat- themes into similar categories; 3) themes were reviewed by the ing transportation vouchers (52%). Table 2 reports mean scores authors; and 4) exemplar quotes were identified for themes by for solutions and exemplar quotes. the authors. An important theme from the open-ended questions cen- tered on technological barriers. Specifically, providers reported data collection concerns (patient-reported outcomes or virtual Results visits) requiring an app, smartphone, or internet access may limit accrual of older adults. Respondents advocated research- Respondent Characteristics ers retaining traditional data collection media (eg, paper and A total of 305 individuals responded to the survey; 50% were pencil, with one respondent stating, “ditch the electronic coordinators, 38% were physicians, 5% were administrators, 3% requirements”) (Table 3). were APPs, and 5% categorized themselves as other. Of the physicians, 13% self-identified as medical oncologists, 12% as an NCORP principal investigators, 6% as an NCORP physician, 4% as a surgeon, and 3% as a radiation oncologist. Seventy- Discussion three percent identified as female. Of the individuals, 76% The review of the literature and the NCORP survey results high- reported age as between 36 and 65 years, 14% were aged light important barriers to clinical trial accrual for older adults younger than 26 years, and 9% were aged older than 65 years. A with cancer in community oncology clinics. Although several of total of 58% reported being in practice for 11 or more years, and these barriers were reported in previous studies focused on 20% identified as members of a community cancer center, 37% accrual of older adults in academic cancer centers, it is impor- identified as being in private practice, and 37% worked in aca- tant to understand the impact of the barriers in community demic medical centers. Of the respondents, 33% characterized oncology clinics where most older adults are cared for. A quali- their practices as 26% to 50% rural, 43% had less than 25% rural tative analysis of medical oncologists (24 academic and 20 from patients, 6% of practices were 76% to 100% rural, and 6% were the community) previously demonstrated differences in per- not rural. ceived barriers; community oncologists were more likely to report that patient understanding and caregiver burden Barriers and Solutions impacted accrual than academic oncologists (14). Given the The top 5 barriers to accrual included comorbidity-attributed increasing focus on electronic methods of data capture and clin- trial ineligibility (84% chose as a top 5 barrier); transportation ical service delivery, an important theme that emerged from issues and the time involved with clinical trial participation this analysis was difficulties with having older adults complete (58%), concern that the proposed regimen is too toxic for older electronic requirements for clinical trial data capture. As these adults (56%), patient or family caregiver declined participation requirements grow in an effort to increase access to trials and (49%), and lack of trials relevant to adult patients (42%). These manage pandemic-related concerns with coming into the office, barriers also had the highest mean scores on the Likert scale for an unintentional and potentially adverse outcome could be a concern (Table 1). Barriers rated relatively less problematic further disparity in accrual of older adults from community included fear of patient compliance, the time required to dis- oncology clinics to cancer clinical trials. cuss or explain a clinical trial to an older adult, physician bias, Eligibility restrictions in protocols are a long-standing barrier requirement for some trials to perform geriatric assessment to accrual of older adults in clinical trials. NCORP survey (GA), and lack of knowledge to assess fitness prior to respondents listed broadening eligibility as the top solution for enrollment. accrual. In one national study of 5499 patients, investigators Qualitative themes regarding barriers included eligibility found that having 1 or more comorbidities was associated with concerns, perceptions that older patients choose less toxic fewer trial discussions and correspondingly less trial participa- treatments than proposed in the clinical trial and want trial tion (15). The American Society of Clinical Oncology and the designs for them specifically (vs accrual onto trials open to any- Friends of Cancer Research have published robust guidelines on one who meets eligibility), impressions that clinical trials are how to develop studies to broaden eligibility with regard to too burdensome for older adults, and concerns that there is not comorbidity, prior therapies, concomitant medications, and sufficient family and caregiver support (Table 1). Clinicians and performance status (16-19). By following this guidance, it is pro- staff reported believing most supportive care trials are too bur- jected that accrual of older adults to clinical trials would densome for older patients and doctors and nurses act as gate- increase (15). Further, guidelines included a recommendation to keepers. Respondents expressed concern over technology include a more optimal functional status evaluation (such as expectations (eg, smartphone availability) and presumed pro- instrumental activities of daily living) when assessing perform- spective enrollees desire paper option for questionnaires. ance status. A robust evidence base indicates oncologists bene- Respondents also expressed that family and caregivers are fit from objective tools to assess the performance status and essential and should be included in the research process as fitness of older adults accurately (20). Clinicians may assume fit much as possible to support patient’s well-being, adherence to older adults are at high risk of adverse outcomes because of Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 120 | J Natl Cancer Inst Monogr, 2022, Vol. 2022, No. 60 Table 1. Barriers with most concern Barrier with most concern Mean (SD) Median (IQR) Range Exemplar quotes Failure to meet clinical trial eligibility require- 3.34 (0.70) 3 (1) 1-5 • “Organ function eligibility requirements may ments because of comorbidities be too strict for older adults eg, creatinine clearance.” • “The single biggest barrier is creatinine clear- ance. I would say that 90% of my patients older than 75 cannot meet the creatinine clearance threshold specified for any study.” • “I have a lot of older adults fail because the lab entry criteria are too strict and they are often mildly anemic and in real life I would treat but would not be allowed in trials.” • “Comorbidities and specifically previous can- cers have been a big issue.” Transportation issues; distance to the treatment 3.09 (0.89) 3 (2) 1-5 • “Lack of payment for hotel and transportation center, time considerations for our rural patients.” • “VA insurance.” • “Lack of CRA support at remote part time rural clinic sites.” • “Time commitment related to a study can be a huge barrier for older adults. They would rather have to spend less time in my setting (hospital).” • “Enrollment takes too long.” Proposed regimen is too toxic for the older adults 3.03 (0.81) 3 (0.75) 1-5 • “In some instances, patients themselves opt for less toxic approaches due to age, performance status, quality of life concerns, and perceived life expectancy.” • “In elderly or patients with many comorbid- ities, they are either ineligible or not suitable for aggressive chemotherapy regimens.” • “Hearing loss is a major barrier to trial enroll- ment in the elderly.” • “Concerns about cognitive capacity for consent.” Patient or family and caregiver preferences not to 2.87 (0.92) 3 (2) 1-5 • “Older patients are choosing not to treat their participate in clinical research cancer.” • “Patients feeling too overwhelmed at new diagnosis.” Lack of trials relevant to older adult patients 2.85 (1.05) 3 (2) 1-5 • “Docs and nurses and clinical staff frequently think supportive care trials are too burdensome for elderly patients and the clinical staff act as barriers and gatekeepers.” patients who are more vulnerable and frailer. A recent system- chronologic age alone. Moreover, many providers mislabel aging-related conditions in older patients who are frailer, lead- atic review demonstrated that one of the most frequent reasons ing to undertreatment of fit older adults and overtreatment of for GA inclusion in clinical trials was the ability to recruit study older adults (21). Clinicians can employ GA to minimize biased participants based on frailty level. Use of GA to evaluate frailty assessment and improve trials assessment and treatment pro- as part of trial eligibility will add information that is normally priety. GA, including shorter screening tools and abbreviated not captured as part of routine oncology performance status versions (20,22,23), provides 2 benefits. First, the GA encourages evaluations (24). GA information can be used to identify patients providers to utilize established, standardized metrics to assess who have characteristics that lead to adverse outcomes from recruitment propriety. Such metrics may refine or correct clini- treatment (2,20). With GA information, clinicians may more cian biases and minimize their influence on trial solicitation. readily, validly, and reliably discern study-eligible patients, Second, these standardized metrics can inform protocol revi- thereby allowing more time for clinicians to promote and dis- sions expanding or restricting eligibility. Evidence-based proto- cuss trials with those truly eligible, and may aid in retention of col revisions, encouraged by reliable and valid GA assessment, older adults to clinical trials (24-26). Workshop participants may increase solicitation frequency, even if revisions reduce advocated for integrating GA into cancer clinical trials to increase accrual of older adults who have patient characteristics the number of study-eligible patients for trials that are designed for fit patients. These data can guide alternative trials for that are more representative of older adults cared for in Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 J. O. Hopkins et al. |121 Table 2. Most supported solution Most supported solution Mean (SD) Median (IQR) Range Exemplar quotes Real-world exclusion criteria including the usual 4.10 (1.01) 4 (1) 1-5 • “Less stringent eligibility criteria related to comorbidities older adults have renal and liver function as well as comorbid- ities would also make it easier to enroll older adults.” • “Definitely need to expand criteria including ECOG to 0-2 or up to 3 if felt to be disease related; CKD and other common comorbidities permitted.” • “Number 1 would be to make inclusion exclu- sion criteria age friendly.” Create trials specifically for the older adults 4.01 (0.98) 4 (1) 1-5 • “Dosage and/or treatment options should be modified to include safer treatment options for elderly participants.” Simplify consent forms 3.79 (1.10) 4 (2) 1-5 • “Simplify things (the consent, provide tools to help patients and their families stay organized or better understand the trial and its activities).” Targeted trial recruitment material for older 3.71 (1.03) 4 (1) 1-5 • “Have a rundown created for each study, show- adults and their family/caregivers ing exactly what would be expected on the study from the patient’s point of view.” • “Support groups—identify other patients who can help ‘mentor’ particularly patients who are widowed and live alone.” • “Generic (not study-specific) research recruit- ment materials noting benefit to future generations.” Provide transportation voucher or gas card for 3.64 (1.13) 4 (2) 1-5 • “Assistance with insurance issues and co-pays trial participants 65 years and older for those on fixed budgets.” • “Transportation vouchers should be done for everyone.” • “Leverage home health, virtual medicine, or other vehicles to fulfill research requirements and data collection while minimizing patient expense, discomfort and burden on family/ support.” CKD ¼ chronic kidney disease; ECS ¼ Eastern Cooperative Oncology Group. community oncology clinics. As one example, a NCI-funded clinicians and staff noted that requiring internet for studies trial evaluating a GA intervention for reducing toxicity, con- would remain a barrier for older adults. There have been data ducted in the NCORP network, enrolled a high prevalence of supporting feasibility of remote (ie, telemedicine) visits for GA, older adults with comorbidities (27,28). These studies provide however, expanding trials into community oncology clinics so evidence that studies designed specifically for older adults that that patients have the ability to participate locally in person integrate GA can be successful and increase accrual of this remains a strong recommendation. Further, in the open-ended underrepresented population. Other manuscripts were devel- questions, NCORP clinicians and staff reported that they had oped by workshop participants for this supplement review opti- concerns with the ability of older adults to complete electronic mal study design for clinical trials and integration of GA into requirements for data reporting, especially patient-reported these trials. outcomes and quality-of-life questionnaires. Several com- The pandemic has increased concerns about the access of mented that offering paper-and-pencil approaches is needed vulnerable groups to clinical trials. There were negative conse- for older adults. Although there is data to support feasibility of quences to oncology clinical trial participation that led to con- remote collection of data for older adults (31), the NCORP survey sideration of the use of technology solutions in an attempt to participant recommendations to “continue to offer QOLs, tutori- maintain equitable participation (29). The NCORP survey dem- als, and other patient materials in paper form vs just electronic” onstrated that transportation issues (because of travel time and should be heeded. Trials should be designed with pragmatic distance as well as need for caregiver support) remain a serious design elements and components, offering flexibility and choice barrier. In another study, a survey of 1183 patients with cancer whenever possible so older patients can choose where they demonstrated that although the majority indicated they would wish to participate and how they wish to provide information. be more likely to participate in a trial if remote technology was Engaging patient and caregivers as research partners when included, older adults were more likely to say they would partic- developing study procedures can foster feasibility with technol- ipate in trials only if they were closer to home (30). NCORP ogy options (32). Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 122 | J Natl Cancer Inst Monogr, 2022, Vol. 2022, No. 60 Table 3. Technology barriers and solutions Barriers Solutions • “Use of technology to collect data (ePRO or virtual visit).” • “Avoid electronic diaries, PROs, etc.” • “Trials require ‘extra work’ that may be considered burdensome or • “Provide nontech options for questionnaires, ie, paper forms com- overwhelming to the elderly, including the use of electronic pleted at clinic visit.” patient reported outcome devices.” • “While technology is great, continue to offer QOLs, tutorials, and • “Having required tech/internet access for needed QOLs.” other patient materials in paper form vs just electronic.” • “Having to use ePRO’s or an app.” • “Please stop creating protocols that require older patients to have • “Study requires patient to use technology, ie, smartphone apps, and be facile with internet participation and other electronic computer-generated questionnaires, video conferencing.” ideas.” • “Many elderly are not willing to do electronic questionnaires or • “Offer PROs on paper as opposed to electronically.” study requirements on an app or smartphone, but much prefer • “Ditch the electronic requirements.” paper forms completed during an office visit.” • “Also, many older adults do not have electronics or do not have the technical skill level to complete study activities online.” ePRO ¼ electronic patient-reported outcome; QOL ¼ quality of life. In addition to reviewing and discussing the survey results, provide a context in which explicit benevolence may mediate the workshop provided a forum for participants to discuss addi- trial recruitment and accrual. tional accrual barriers, notably implicit or unintentional bias, In circumstances where there is limited evidence for safety and explored strategies that may mitigate this presumed clini- and efficacy, clinicians may more readily rely on clinical experi- ence when considering accrual of older adults to clinical trials. cal trial barrier. Workshop participants additionally discussed how engagement of clinical staff could improve clinical trial Clinicians relying on erroneous estimates may demonstrate an accrual of older adults. “insensitivity to prior probability of outcomes” (41). Specifically, clinicians potentially evaluate the likelihood a patient is study eligible or ineligible referencing the degree to which the patient exhibits an exclusion criterion–relevant stereotype. For exam- Bias Related to Accrual of Older Adults to Clinical Trials ple, clinicians may unconsciously label all or most older adults Bias is a stereotype that leads to a distorted judgment nega- as frail because the majority of their frail patients are older. tively impacting an already disadvantaged group (33-36). This insensitivity potentially begets the “explicit[ly] benevolent” Aspects of clinician bias may reflect well-intended aspirations stance, “I believe older adult patients are frail. I aspire to do no designed to protect or advance disadvantaged groups. Results harm and protect my patients. Therefore, I will not subject my from the survey support that respondents believe that clinicians older adult patients to [a given] clinical trial and decline to and staff act as gatekeepers for trial enrollment. This “explicit recruit this patient.” Although clinicians intend to do no harm, benevolence” may reinforce the very disparity well-intended these beliefs stem from age-related stereotypes (ie, ageism) that perpetuate inequities (35,42). Addressing this perspective is a clinicians aspire to mitigate. For older adults, explicit benevo- lence manifests during the assessment of patients’ trial eligibil- prerequisite to trial design innovation. Indeed, pragmatic trials ity (a clinician-level consideration). Clinicians intend to first, do may hold promise for increasing accessibility, assuaging no harm. Where uncertain about trial propriety (ie, patient fit- resource use, and imposing less patient burden (43). However, ness and/or concerns about toxicity), clinicians may err toward study design and inclusion criteria pragmatism, though neces- exclusion, not solicitation. Further, clinicians align both patient sary, may still fail to address the clinician’s interpretation of the care and trial accrual principles on tenets of justice, benefi- inclusion criteria. Consequently, clinicians may employ well- cence, and respect for persons. When contemplating trial meaning, but flawed, exclusionary defaults, regardless of a recruitment, clinicians consider whether a trial advances or study (or inclusion criteria’s) pragmatic qualities. deprives a patient of care that the provider deems essential or Addressing explicit benevolence and/or bias is challenging. Systemic modifications to clinical trials, including expansion of asks patients to undergo increased burden (justice). Clinicians commit to securing patients’ well-being, which includes maxi- inclusion criteria, will not produce change unless individual mizing benefit and minimizing harm (beneficence). Finally, clinicians acknowledge inherent biases and, once recognized, clinicians aspire to affirm patients’ autonomy and to protect change behavior. By reflecting on biases, clinicians can critically examine their own opinion of a study’s capacity to advance those less positioned to act independently (respect for persons). These aspirational classifications potentially motivate an clinical practice. Clinicians can constructively articulate their explicit benevolence that blunts trial solicitation and accrual. In concerns to investigative teams, including study sponsors and addition, the care encounter is fraught with competing the principal investigators (PIs). Likewise, study teams can demands and perceptions that mitigate trial engagement actively engage community oncology stakeholders to co- (1,37,38). Those particularly germane to trial accrual include develop trials prioritizing older adult recruitment. Apart from provider belief that their organization does not value research sponsor and PI education, these discussions also encourage enough to credit in career advancement considerations, lack of clinician and practice ownership, responsibility, and account- access to research training, perceived inability to influence ability for accrual effort. Such discussions potentially discour- practice through research, and belief that research teams age provider rationalization (eg, “This study is too difficult”) by identifying solutions early in trial development. Clinicians can underestimate the time required to execute research tasks (39,40). Thus, competing care demands and cultural barriers also communicate their opinions on a study’s value thereby Downloaded from https://academic.oup.com/jncimono/article/2022/60/117/6908746 by DeepDyve user on 20 December 2022 J. O. Hopkins et al. |123 directing sponsor and PI efforts from potentially futile protocol practices. Although the workshop discussed long-standing bar- amendments. Information gleaned from this transparency riers to accrual, we were able to identify solutions that could allows PIs to tailor studies, particularly recruitment, to practice facilitate accrual of older adults to NCI-funded clinical trials in and/or organization characteristics to improve recruitment. PIs community oncology clinics; this information will guide inter- can use this feedback to transition from patient-focused inclu- ventions and efforts led by the NCI to improve accrual of older sion criteria (eg, age, disease status) to multilevel inclusion cri- adults to clinical trials. Consequently, we encourage interven- teria that include matching studies to clinician and practice tions targeting patient, providers, families and caregivers, and resources, culture, and goals (40). Such an approach may restrict organizations in which care teams contemplate trial propriety. site availability but maximize recruitment at the sites electing Ultimately, stakeholders must also consider the community to participate. Multilevel research is needed to rigorously assess context and sociopolitical landscape that informs, reinforces, the merits of these potential approaches (44). and rewards organizational structures, policies, and activities that inherently impede accrual of older adults to NCI-funded cancer clinical trials. Clinician and Staff Engagement as a Mechanism to Increase Enrollment of Older Adults to Clinical Trials Funding The previous 20 years produced an explosion of APPs including This study received funding from the National Cancer nurse practitioners, physician’s assistants, and clinical pharma- Institute (UG1CA189961 for the URCC NCORP Research Base cists, who more directly participate in oncology patient care, and UG1CA189804 for the Hawaii Minority/Underserved including older adults. APPs report interest in increasing their NCORP) and the National Institute on Aging (K24AG056589, participation in clinical research and desire inclusion in clinical R33AG059206 to SGM). trials teams (45,46). Therefore, APPs may help address staffing- attributed accrual barriers. Additionally, APPs can facilitate edu- cation for older adults and caregivers, and this education may Notes better ensure informed decisions regarding clinical research participation. Role of the funder: The funder, the NIH, is a sponsor for the con- Clinicians express concern about extra time required to ference and for all the manuscripts in the Monograph. This enroll patients onto trials; however, they may mitigate this bar- manuscript is a collaboration between investigators and NIH rier by employing a team approach. For example, an oncologist employees. may introduce the study as part of the standard of care, and Disclosures: There are no disclosures to report for any of the then the APP subsequently educates the patient on the treat- authors. ment and describes the clinical trial option. For patients expressing interest, the APP can solicit the clinical research Author contributions: Conceptualization all; Funding acquisi- coordinator to more explicitly describe the trial to the patient tion DS; Data collection DS, SM; Project administration SM, MW; and family. This team approach can lessen accrual burden Data analysis SM, SG, KM, MW; Data interpretation all; Writing among team members and may allay the “time and burden to all except DS; Writing review all. enroll” (47). APPs and nurses also report routinely providing patient care coordination, follow-up visits, and toxicity checks as part of their daily practice for older patients with cancer (48). Data Availability Care teams typically include APPs and nurses particularly posi- tioned to address the identified barriers (eg, toxicity manage- Data (ie, survey responses) were collected by NIH and reported ment, visit coordination) (49). in aggregate. The University of Rochester NCI Community Forty years of research reveals suboptimal accrual of older Oncology Research Program Research Base analyzed the data. adults in clinical trials, with investigators identifying barriers No identifiers were collected. Raw aggregate data can be and proposing solutions. 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JNCI Monographs – Oxford University Press

Published: Dec 15, 2022

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