Skip to main content
NCBI home page
JCO Oncology Practice logoLink to JCO Oncology Practice
. 2020 Apr 2;16(9):e849–e858. doi: 10.1200/JOP.19.00662

Barriers to Participation in Therapeutic Clinical Trials as Perceived by Community Oncologists

Andrew R Wong 1, Virginia Sun 2, Kevin George 1, Jennifer Liu 1, Simran Padam 1, Brandon A Chen 1, Thomas George 1, Arya Amini 3, Daneng Li 1, Mina S Sedrak 1,✉
PMCID: PMC7489483  PMID: 32240068

Abstract

PURPOSE:

Despite considerable research on the barriers to enrollment in cancer therapeutic trials, few studies have elicited barriers from the perspective of community physicians, who provide the majority of cancer care. The purpose of this study was to characterize barriers to and facilitators of cancer therapeutic trials as perceived by oncologists in community practices.

METHODS:

Twenty semistructured interviews were conducted with oncologists at six community sites affiliated with City of Hope National Medical Center from March to June 2018. Responses were recorded digitally and transcribed. Data were analyzed using qualitative content analysis.

RESULTS:

Of the 20 participants, 4 (20%) were women, 13 (65%) had > 10 years of practice experience, and 16 (80%) reported that < 5% of their patients were enrolled in a therapeutic trial. Participants identified four system-level barriers: lack of appropriate trials for community-based settings, insufficient infrastructure support, restrictive eligibility criteria, and financial limitations; three physician-level barriers: lack of awareness of available trials, lack of knowledge of trial details, and lack of time; and two patient-level barriers: patient burden and negative beliefs/attitudes toward research. Efforts aimed to increase trial availability, clinical trial support personnel, and physician knowledge were identified as major facilitators.

CONCLUSION:

Community oncologists face numerous complex, multifaceted barriers to cancer therapeutic trial enrollment. Although expanding clinical research beyond the academic setting allows access to a larger and more diverse patient population, increasing generalizability and relevance of trial findings, there remains a substantial need for new strategies to improve cancer research delivery in the community.

INTRODUCTION

Over the past three decades, the dramatic progress in treating cancer has been driven predominantly by clinical trials designed to identify new, more effective therapies.1,2 However, patient participation in cancer therapeutic trials remains a major challenge, as < 5% of adult patients with cancer enroll in therapeutic studies.3 Barriers to cancer clinical trial enrollment have been frequently studied, yet trial participation rates have not improved significantly over time.4 Addressing this problem is important to improve the generalizability of trial results,5 minimize the premature closure of trials,6 and prevent delays in the advancement of new cancer therapies.7

Several studies have identified barriers to trial participation faced by multiple stakeholders, including physicians,8-11 patients,12-14 and research personnel.15,16 However, most studies have focused on academic-based research settings, and few have investigated the unique challenges faced in community practice. Understanding these barriers is an important and unmet need, given that nearly 80% of patients receive their cancer care in community settings.17,18 Furthermore, barriers in community-based cancer research may vary from those in academic-based research because of differences in patient volume,19,20 physician responsibilities,19,21 and clinical trial infrastructure (eg, personnel).22,23

To date, most studies assessing barriers in the community-based oncology practice have primarily been retrospective reviews and surveys of physicians’ perceptions of barriers.8-11,13-15 Few studies have used qualitative methods to examine community oncologists’ perceptions of the barriers and potential facilitators to address those barriers.16,24,25 Knowledge of the nuances surrounding the complex challenges with therapeutic trial enrollment in the community is an important step toward designing and evaluating interventions to improve accrual. To fill this knowledge gap, we conducted semistructured interviews with community oncologists to elicit their perspective of the barriers to and facilitators of patient participation in cancer therapeutic trials.

METHODS

Study Design and Setting

Semistructured interviews were conducted from March to June 2018 with 20 community medical oncologists at six City of Hope (COH)–operated community practices. COH is an independent research and treatment center for cancer. It is composed of a main campus, located in Duarte, California, 21 miles northeast of Los Angeles, and 29 COH-operated community practices, stretching from Palm Springs to the east and Simi Valley to the west (150 miles), and Lancaster to the north and Corona to the south (65 miles). In this study, participants were recruited from six of the 29 COH-operated community sites; the average distance between these six sites and the main campus was 34 miles (range, 7-81 miles). At the time of this study, clinical research at COH was conducted at both the main campus and these six sites, with approximately one-fourth of all active therapeutic trials on the main campus being available in these community sites. Sites had an average of four medical oncologists per practice (range, two to six). Five of the six sites had at least one dedicated clinical research personnel to support the conduct of clinical trials. Across the six sites, the mean patient age was 63 years (median, 65 years; range, 1-107 years), 19% identified as nonwhite race, 21% were Hispanic, and 20% did not speak English as their primary language. The study was deemed exempt by the institutional review board. Findings were reported using the Consolidated Criteria for Reporting Qualitative Research (COREQ) reporting guidelines (Data Supplement).26

Participant Selection

Oncologists from the six community sites were invited via e-mail to participate in telephone or face-to-face interviews. We approached 23 community oncologists. Twenty (87%) agreed to participate and completed the interview (six out of six oncologists at site A, five out of six oncologists at site B, four out of four at site C, two out of two at site D, two out of three at site E, and one out of two at site F). One declined because of lack of time, and two did not respond to the e-mail invitation.

Data Collection

An interview guide was developed, based on an a priori framework, after a literature review of the barriers and facilitators to cancer clinical trial enrollment.27-47 The interview guide included prompts and was used flexibly to allow participants’ perspectives to be explored in depth. After initial development, a preliminary version of the guide was used to conduct a pilot interview with one oncologist, which was not included in the final analysis. On the basis of pilot interview feedback, the guide was revised iteratively by the study team (Appendix, online only).

One male research assistant with a Bachelor of Science degree and training in qualitative research methodology (K.G.) conducted all semistructured interviews with each participant individually. The investigator had no direct relationship with the participants before the study, and participants were interviewed only once. Nineteen interviews were completed over the phone and one was conducted in person in a private room at COH. Before the interviews, participants were informed of the purpose of the research and were given a written statement that included all the elements of informed consent.

All interviews were audio recorded using a digital recorder and transcribed verbatim by one investigator (K.G.).48 Field notes were collected during and/or after the interviews. Two separate investigators (A.R.W., S.P.) reviewed the transcripts to ensure the quality and accuracy of the transcriptions. Personal information was removed from the transcripts before analysis to ensure confidentiality. Transcripts were not returned to participants for comment or correction.

Data Analysis

All data were collected and managed using qualitative analysis software (NVivo 12; QSR International, Melbourne, Australia). Transcripts were continuously reviewed and assessed for the emergence of new themes without a predetermined theory or framework. Thematic content analysis was used to inductively code the transcripts.49 Two investigators (K.G., A.R.W.) independently coded all transcripts to identify codes and themes; discordant coding was discussed and adjudicated by consensus. Participants were not invited to provide feedback on findings. Content analysis generated major themes and subthemes. Regular discussions on the findings were conducted among the study team to ensure methodological rigor.50 Two investigators with qualitative analysis experience (V.S., M.S.S.) conducted a final validation review of the themes to ensure consistency and clarity. Results were reported using direct quotes from interviews,51 details were provided on the sample and setting,52 and findings were related to other literature.53

RESULTS

Among the 20 participants, four (20%) were women, and 13 (65%) had > 10 years of practice experience. Sixteen (80%) reported that < 5% of their patients were enrolled in clinical trials (Table 1). Interviews ranged from 6 to 33 minutes (median, 11 minutes). Factors that influence clinical trial enrollment in community oncology practices clustered around three major domains: system and protocol factors, physician factors, and patient factors (Tables 2 and 3).

TABLE 1.

Oncologist and Practice Characteristics (N = 20)

graphic file with name JOP.19.00662t1.jpg

Open in a new tab

TABLE 2.

Oncologists’ Perceptions of Barriers in Cancer Clinical Trials: Identified Themes and Representative Quotes

graphic file with name JOP.19.00662t2.jpg

Open in a new tab

TABLE 3.

Oncologists’ Perceptions of Facilitators in Cancer Clinical Trials: Identified Themes and Representative Quotes

graphic file with name JOP.19.00662t3.jpg

Open in a new tab

System and Protocol Factors

Within the system and protocol domain, four themes were identified as key barriers to clinical trial participation in the community: (1) lack of appropriate trials for community-based settings, (2) insufficient infrastructure support, (3) restrictive eligibility criteria, and (4) financial limitations.

Lack of appropriate trials for community-based settings.

Participants commonly noted that available clinical trials often do not match the disease types and stages of patients treated in the community. For example, one participant emphasized that many trials are designed to treat patients at academic sites, who often have diseases that differ from those of patients in the community. “Our goals differ from … [those of] tertiary, academic centers. More of our patients come in requiring adjuvant therapy [or] first-line metastatic trials. Those are the trials we like [and need] … whereas the academic center ... tend[s] to see patients [receiving] fourth- or fifth-line” (participant 3 [P3]). One participant identified that trial availability and “having a fairly robust [clinical trial] portfolio” (P1) was a main facilitator of enrollment.

Insufficient infrastructure support.

Even when trials are available and appropriate for patients, participants reported difficulty accruing because of insufficient research support. Specifically, limited community-based clinical trial infrastructure was identified as a major barrier to enrollment. “We only have two people in our office for [all] trials,” noted one participant; “they are drowning in paperwork, are overwhelmed, [and] are not always available to talk with the patient with a potential trial” (P6). Several participants noted that increasing research personnel support is a key facilitator. Staff with familiarity of available trials and dedicated time to enroll and monitor patients was a commonly cited need. “[The research coordinator] goes over my patients and if she sees anyone potentially eligible … she will let me know about it” (P16).

Restrictive eligibility criteria.

Participants noted that when potential patients were screened for eligibility, strict inclusion/exclusion criteria often served as a barrier to enrollment. “Trials require … perfect patients, which [are] nowhere to be found” (P19). Many participants expressed that broader eligibility criteria are necessary to include a more diverse patient population, representative of the patients seen in practice.

Financial limitations.

Even when an eligible patient was identified, the lack of financial coverage for trial participation by common insurance plans, such as health maintenance organizations (HMOs), was reported as a barrier to enrollment in the community. “HMOs are reluctant to put patients on trial, probably because of financial reasons” (P7). Participants noted that trials ought to be designed to mitigate patients’ financial burden. For example, one participant noted that trials that provided payment for the study drug and/or minimized costly restaging scans might facilitate higher trial enrollment than other trials.

Physician-Related Factors

Within the physician-related domain, three themes were identified as barriers: (1) lack of awareness of available trials, (2) lack of knowledge of trial details, and (3) lack of time.

Lack of awareness of available trials.

Participants expressed difficulty in staying aware of all available clinical trials. One participant reported that this challenge is uniquely prevalent in the community because physicians in the community treat a variety of tumor types, whereas physicians in academic settings often treat one tumor subtype. “I am treating all types of cancers … there are a lot of different trials and it is difficult to keep them all straight in my mind” (P5). To remain knowledgeable of available trials, participants cited several resources, including educational material (eg, pamphlets, e-mails, and websites). “[My] main resource is that [my institution] has a list of clinical trials that they update … there is [also] a website where you can type in different malignancies and [identify] available trials” (P5). Others reported that their colleagues prompt them to consider clinical trials. “If my colleague came to me saying ‘I have this new trial that I’m really interested in’ … then I’m all ears” (P1). Many participants reported being prompted to consider clinical trials when their patients progress from standard-of-care treatment. “When a person progresses … I start thinking about switching therapy. That is one of the main … triggers to think about a trial” (P6). Prior or ongoing clinical expertise was also identified as a facilitator of knowledge of available trials. “I did mostly breast cancer, so I knew almost every trial inside and out” (P15).

Lack of knowledge of trial details.

Even when participants were aware of available trials, they commonly reported the challenge of knowing specific trial details. “To tell your patient ‘Okay, the investigational drug is this, and these are the side effects, and this is how you take it,’ you have to read a lot of information” (P6). Participants cited that they are more likely to consider trials if they have a clear understanding of the potential promise, benefit, and toxicity of the investigational agent. “[Clinical trials] embed themselves in [a physician’s] mind better if [physicians] know that [a trial] really suits their need to provide for their patients” (P1).

Lack of time.

“In the community … our practice is so busy, it takes time to investigate whether the patient is eligible, or if there is a potential clinical trial for the patient, [and hence] there is a temptation to use standard-of-care treatments without necessarily exploring clinical trial options” (P9). Participants noted that being prompted by research personnel and patients is a facilitator. “[It’s helpful] having patients in front of me specifically asking what trials are available” (P5).

Patient-Related Factors

Within the patient-related domain, two themes were identified as barriers: (1) patient burden, and (2) negative beliefs/attitudes toward cancer research.

Patient burden.

“Trials are complicated … sometimes they require invasive procedures … [this] is a barrier for the patient in two respects. One is [patients] have to go through another procedure … [which leads to] pain and potential complications. [Two is] it delays the treatment” (P14). In particular, participants highlighted distance to access clinical trials as a patient burden, particularly for patients from lower income and/or rural areas. “I have patients who come from Needles [rural California]. That’s 3 to 4 hours away. For them to get on the clinical trial with COH, for example, it would be challenging” (P1). Having a budget dedicated to addressing transportation burden was cited as a potential facilitator.

Beliefs/attitudes.

Other participants reported that some patients held negative attitudes toward clinical trial participation, such as equating clinical trials with experimentation. “Twenty-five percent [of patients] would say, ‘I am not going to be a guinea pig’ and that would be the end … the idea of being on a clinical trial likens them to a research animal, which I think they are offended by” (P1). Participants identified a need for increased patient education of the purpose and importance of cancer therapeutic trials.

DISCUSSION

In this study, we elicited physician perceptions of the barriers to and facilitators of patient participation in cancer therapeutic trials in community settings. Our findings reveal that community oncologists face numerous complex, multifaceted barriers. Lack of appropriate trials for their patient population, insufficient infrastructure support, and increased physician burden were identified as the major factors that influence trial participation.

Despite considerable research on the barriers to enrollment in cancer therapeutic trials, few studies have explored barriers within the community setting, where the majority of patients with cancer are treated.16,24,25 Of the studies that have explored barriers in the community, most have primarily been retrospective reviews and surveys of physicians’ perceptions of barriers, and the majority of these focused on cancer control, prevention, and care delivery trials.8-11,13-15 Few studies have used qualitative methods to explore the nuances surrounding the complexity of expanding cancer therapeutic trials in the community, and our findings add to the current literature by providing an in-depth understanding of physicians’ perceptions of the critical and unmet needs to facilitate patient participation in cancer treatment trials in the community.

Although academic cancer centers play a crucial role in clinical research, the majority of cancer care takes place in the community setting, and our findings underscore that existing cancer therapeutic trials may not be designed to answer questions relevant to patients with cancer treated in the community. Expanding clinical research beyond the academic environment allows access to a larger and more diverse patient population treated in a variety of health care delivery settings, which can accelerate accrual to cancer clinical trials and increase the generalizability of trial findings. However, most clinical trials are driven by scientific priorities, ethical and regulatory considerations, and profit potential, rather than implementation of research advances into practice. Community oncologists highlight a disconnect between the available trials and their patient needs.27 For example, participants in this study often noted that few treatment trials were available for patients receiving first-line metastatic or adjuvant treatments, who make up a large proportion of the patient population that they see in practice. Efforts to engage community oncologists in the entire life cycle of cancer treatment trials, from early development and design stages to delivery approaches that can be implemented in the usual clinical workflow, are needed.54 Furthermore, ongoing efforts are underway to broaden the eligibility criteria and facilitate patient access to treatment trials, but it is too early to know to what extent these initiatives will help foster more appropriate and available trials in the community.5

Furthermore, our findings highlight the need for improved clinical trial infrastructure in the community. Our interviews with community oncologists elicited important insights about the complexity of cancer research delivery in the community. For example, research personnel are often understaffed and overburdened, with limited access to educational materials, such as websites and handouts, which are not frequently updated or accurate. Furthermore, oncologists noted limited time, knowledge, and awareness of trials, which is confounded by concerns that trials will increase patients’ burdens (eg, lack of transportation, limited insurance coverage) and/or require additional efforts to address many of the negative attitudes patients have toward research. The majority of themes identified in our study underscore that there is insufficient infrastructure to facilitate seamless cancer research delivery within the usual clinical workflow in the community settings.56 Efforts to increase clinical trial support within community sites are urgently needed, given the ongoing national movement of large academic medical centers expanding patient care and clinical research to partner community sites.57-59 Examples of these efforts include the National Cancer Institute (NCI) Community Cancer Centers Program, a short-term pilot that ended in the early 2010s, which showed that increased personnel support can improve clinical trial enrollment in the community60,61; and clinical trial navigation services, such as oncology nurse navigators, for patients from underserved groups to connect with patient advocacy groups62 and publicly available support resources and culturally sensitive education material.63,64 However, building research infrastructure will likely become more challenging as value-based reimbursement efforts grow. Additional research and policies are necessary to understand whether investments in clinical trial resources are sustainable models of care that can lead to robust accrual in the community settings.

There are several limitations to this study. First, there may be limited generalizability of study findings because this study was conducted with physicians at sites affiliated with a single institution that has a dedicated interest in conducting clinical trials. As a result, our findings may not be representative of community sites that have no affiliation with an academic center. Second, we did not probe oncologists to distinguish the association between trial sponsors (eg, NCI v industry) and barriers to enrollment. Distinct differences between various trial sponsors may influence barriers and facilitators to clinical trials; for example, industry-sponsored trials may be better resourced and thus may allow for more infrastructure support than nonindustry-sponsored trials. Third, this study is potentially susceptible to bias because physicians may have felt obligated to overplay the facilitators and underplay the barriers they face to clinical trial accrual to the interviewer, who is also a member of the institution. To minimize potential bias, we ensured confidentiality by guaranteeing the de-identification of interview data. Finally, this is hypothesis-generating research based on a qualitative analysis. Therefore, we are unable to make claims beyond reporting the perceptions of interviewees. Despite these limitations, this study provides important insights that may inform the design of interventions to improve cancer clinical trial accrual in the community setting.

In the era of genomics and molecularly targeted therapy, the shift toward precision oncology may necessitate a shift to integrate clinical trials into the daily operations of patient care. This is not a simple undertaking, but it is an important and urgent one. Our findings highlight an enormous need for more research, policies, and strategies to remove known obstacles to patient participation in cancer therapeutic trials in the community setting. Substantial steps are needed to ensure that clinical research is successful in the community and that modifiable barriers to participation are addressed. Only then will expanding clinical research into the community serve to improve patient access to trials, accelerate enrollment, and strengthen the impact of clinical research.

ACKNOWLEDGMENT

We thank Kerin Higa for providing critical revisions of the manuscript for important intellectual content.

Appendix

Interview Guide

Introduction.

Thank you for agreeing to participate in this interview study. I expect that the interview will take approximately 15-20 minutes to complete.

The purpose of the interview is to explore barriers to enrolling patients on clinical trials and facilitators that you think may improve accrual. We are interested in learning more about your experiences as a medical oncologist who is involved in clinical trials. Your opinions are extremely valuable to us as we look for ways to improve clinical trial participation.

I will be recording the interview. Your responses will be recorded digitally and transcribed. Personal information will be removed before analysis to ensure confidentiality. All digital audio files will be deleted after transcription. I would ask you to please refrain from using any patient-identifying information during our conversation. Your participation is entirely voluntary and you may refuse to participate or discontinue the interview at any time without penalty. By completing the interview, you have consented to our use of the information you provide.

Do you have any questions before we begin? If you agree, I will now turn on the recorder and we will begin the interview.

[Interviewer will turn on the recorder.]

The recorder is now on.

First, I’d like to know about your general experience with cancer clinical trials.

  1. How many years have you been practicing as a medical oncologist?

  2. Approximately how many patients are in your patient panel? How many of your patients have ever participated or currently participate in a clinical trial?

  3. In the care of a patient with cancer, what typically will prompt you to consider a clinical trial?

  4. What information sources do you use to learn about clinical trials that your patients may be eligible for? Why do you use these sources as opposed to others?

  5. How would you rate your confidence about knowing what trials are available for any one particular patient? Would you care to expand on why you answered this way?

Next, I’d like to know a little bit about your experience with leading clinical trials.

  1. Have you been a Principal Investigator on any clinical trials? If so, how many?

  2. Thinking back to your experience leading these trials, how did you (or your team) find patients for your trials? Did you use any tools to promote your trial among your peers? What about the public?

  3. How significant of a problem was patient recruitment overall on trials you have led?

    • What do you think are some of the root causes for difficulties accruing patients?

    • What do you think makes some trials easier to accrue to? Harder to recruit to?

Thank you again for your contribution. If you have any questions, please feel free to contact us using the contact information provided on the Statement of Research.

PRIOR PRESENTATION

Presented at the American Society of Clinical Oncology annual meeting, Chicago, IL, May 31-June 4, 2019.

SUPPORT

Supported in part by the National Cancer Institute Grant No. NCI K12CA001727 (M.S.S.), the National Institute of Aging Grant No. NIA R03AG064377 (M.S.S.), the Waisman Innovation Fund, and Circle 1500.

The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; or the decision to submit the manuscript for publication.

AUTHOR CONTRIBUTIONS

Conception and design: Virginia Sun, Kevin George, Arya Amini, Mina S. Sedrak

Financial support: Mina S. Sedrak

Administrative support: Mina S. Sedrak

Collection and assembly of data: Andrew R. Wong, Kevin George, Simran Padam, Mina S. Sedrak

Data analysis and interpretation: Andrew R. Wong, Virginia Sun, Kevin George, Jennifer Liu, Simran Padam, Brandon A. Chen, Thomas George, Daneng Li, Mina S. Sedrak

Manuscript writing: All authors

Final approval of manuscript: All authors

Accountable for all aspects of the work: All authors

AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

Barriers to Participation in Therapeutic Clinical Trials as Perceived by Community Oncologists

The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated unless otherwise noted. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO's conflict of interest policy, please refer to www.asco.org/rwc or ascopubs.org/op/site/ifc/journal-policies.html.

Open Payments is a public database containing information reported by companies about payments made to US-licensed physicians (Open Payments).

Arya Amini

Consulting or Advisory Role: RefleXion Medical

Speakers' Bureau: AstraZeneca

Daneng Li

Consulting or Advisory Role: Lexicon, Ipsen, Exelixis, Bayer, Eisai, Taiho Pharmaceutical, Genentech

Speakers' Bureau: Lexicon, Ipsen, Advanced Accelerator Applications, Exelixis, Eisai

Research Funding: Brooklyn ImmunoTherapeutics (Inst)

Mina S. Sedrak

Research Funding: Novartis (Inst), Seattle Genetics (Inst)

No other potential conflicts of interest were reported.

REFERENCES

  • 1.DeMets DL, Califf RM. A historical perspective on clinical trials innovation and leadership: Where have the academics gone? JAMA. 2011;305:713–714. doi: 10.1001/jama.2011.175. [DOI] [PubMed] [Google Scholar]
  • 2.Unger JM, Nghiem VT, Hershman DL, et al. Association of National Cancer Institute-sponsored Clinical Trial Network group studies with guideline care and new drug indications. JAMA Netw Open. 2019;2:e1910593. doi: 10.1001/jamanetworkopen.2019.10593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Virani S, Burke L, Remick SC, et al. Barriers to recruitment of rural patients in cancer clinical trials. J Oncol Pract. 2011;7:172–177. doi: 10.1200/JOP.2010.000158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Murthy VH, Krumholz HM, Gross CP. Participation in cancer clinical trials: Race-, sex-, and age-based disparities. JAMA. 2004;291:2720–2726. doi: 10.1001/jama.291.22.2720. [DOI] [PubMed] [Google Scholar]
  • 5.Elting LS, Cooksley C, Bekele BN, et al. Generalizability of cancer clinical trial results: Prognostic differences between participants and nonparticipants. Cancer. 2006;106:2452–2458. doi: 10.1002/cncr.21907. [DOI] [PubMed] [Google Scholar]
  • 6. Tang C, Sherman SI, Price M, et al: Clinical trial characteristics and barriers to participant accrual: The MD Anderson Cancer Center experience over 30 years, a historical foundation for trial improvement. Clin Cancer Res 23:1414-1421, 2017. [DOI] [PMC free article] [PubMed]
  • 7.Bennette CS, Ramsey SD, McDermott CL, et al. Predicting low accrual in the National Cancer Institute’s Cooperative Group clinical trials. J Natl Cancer Inst. 2015;108:djv324. doi: 10.1093/jnci/djv324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Mahmud A, Zalay O, Springer A, et al. Barriers to participation in clinical trials: A physician survey. Curr Oncol. 2018;25:119–125. doi: 10.3747/co.25.3857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Manne S, Kashy D, Albrecht T, et al. Attitudinal barriers to participation in oncology clinical trials: Factor analysis and correlates of barriers. Eur J Cancer Care (Engl) 2015;24:28–38. doi: 10.1111/ecc.12180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Kemeny MM, Peterson BL, Kornblith AB, et al. Barriers to clinical trial participation by older women with breast cancer. J Clin Oncol. 2003;21:2268–2275. doi: 10.1200/JCO.2003.09.124. [DOI] [PubMed] [Google Scholar]
  • 11.Somkin CP, Ackerson L, Husson G, et al. Effect of medical oncologists’ attitudes on accrual to clinical trials in a community setting. J Oncol Pract. 2013;9:e275–e283. doi: 10.1200/JOP.2013.001120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Mills EJ, Seely D, Rachlis B, et al. Barriers to participation in clinical trials of cancer: A meta-analysis and systematic review of patient-reported factors. Lancet Oncol. 2006;7:141–148. doi: 10.1016/S1470-2045(06)70576-9. [DOI] [PubMed] [Google Scholar]
  • 13.Lara PN, Jr, Higdon R, Lim N, et al. Prospective evaluation of cancer clinical trial accrual patterns: Identifying potential barriers to enrollment. J Clin Oncol. 2001;19:1728–1733. doi: 10.1200/JCO.2001.19.6.1728. [DOI] [PubMed] [Google Scholar]
  • 14.Hamaker ME, Seynaeve C, Nortier JW, et al. Slow accrual of elderly patients with metastatic breast cancer in the Dutch multicentre OMEGA study. Breast. 2013;22:556–559. doi: 10.1016/j.breast.2012.12.010. [DOI] [PubMed] [Google Scholar]
  • 15.Vanhoff D, Hesser T, Kelly KP, et al. Facilitating accrual to cancer control and supportive care trials: The clinical research associate perspective. BMC Med Res Methodol. 2013;13:154. doi: 10.1186/1471-2288-13-154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Grunfeld E, Zitzelsberger L, Coristine M, et al. Barriers and facilitators to enrollment in cancer clinical trials: Qualitative study of the perspectives of clinical research associates. Cancer. 2002;95:1577–1583. doi: 10.1002/cncr.10862. [DOI] [PubMed] [Google Scholar]
  • 17.American Society of Clinical Oncology The state of cancer care in America, 2014: A report by the American Society of Clinical Oncology. J Oncol Pract. 2014;10:119–142. doi: 10.1200/JOP.2014.001386. [DOI] [PubMed] [Google Scholar]
  • 18.Nabhan C, Jeune-Smith Y, Klinefelter P, et al. Challenges, perceptions, and readiness of oncology clinicians for the MACRA quality payment program. JAMA Oncol. 2018;4:252–253. doi: 10.1001/jamaoncol.2017.3773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Desch CE, Blayney DW. Making the choice between academic oncology and community practice: The big picture and details about each career. J Oncol Pract. 2006;2:132–136. doi: 10.1200/jop.2006.2.3.132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Shanafelt TD, Gradishar WJ, Kosty M, et al. Burnout and career satisfaction among US oncologists. J Clin Oncol. 2014;32:678–686. doi: 10.1200/JCO.2013.51.8480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Tsang JLY, Ross K. It’s time to increase community hospital-based health research. Acad Med. 2017;92:727. doi: 10.1097/ACM.0000000000001681. [DOI] [PubMed] [Google Scholar]
  • 22.Carey M, Boyes AW, Smits R, et al. Access to clinical trials among oncology patients: Results of a cross sectional survey. BMC Cancer. 2017;17:653. doi: 10.1186/s12885-017-3644-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Likumahuwa S, Song H, Singal R, et al. Building research infrastructure in community health centers: A Community Health Applied Research Network (CHARN) report. J Am Board Fam Med. 2013;26:579–587. doi: 10.3122/jabfm.2013.05.130025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Go RS, Frisby KA, Lee JA, et al. Clinical trial accrual among new cancer patients at a community-based cancer center. Cancer. 2006;106:426–433. doi: 10.1002/cncr.21597. [DOI] [PubMed] [Google Scholar]
  • 25.Davis TC, Arnold CL, Mills G, et al. A qualitative study exploring barriers and facilitators of enrolling underrepresented populations in clinical trials and biobanking. Front Cell Dev Biol. 2019;7:74. doi: 10.3389/fcell.2019.00074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Tong A, Sainsbury P, Craig J. Consolidated criteria for reporting qualitative research (COREQ): A 32-item checklist for interviews and focus groups. Int J Qual Health Care. 2007;19:349–357. doi: 10.1093/intqhc/mzm042. [DOI] [PubMed] [Google Scholar]
  • 27.Unger JM, Vaidya R, Hershman DL, et al. Systematic review and meta-analysis of the magnitude of structural, clinical, and physician and patient barriers to cancer clinical trial participation. J Natl Cancer Inst. 2019;111:245–255. doi: 10.1093/jnci/djy221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Cummings FJ, Gelman R, Tormey DC, et al. Adriamycin plus vincristine alone or with dibromodulcitol or ICRF-159 in metastatic breast cancer. Cancer Clin Trials. 1981;4:253–260. [PubMed] [Google Scholar]
  • 29.das Nair R, Orr KS, Vedhara K, et al. Exploring recruitment barriers and facilitators in early cancer detection trials: The use of pre-trial focus groups. Trials. 2014;15:98. doi: 10.1186/1745-6215-15-98. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Hawkins BS, Prior MJ, Fisher MR, et al. Relationship between rate of patient enrollment and quality of clinical center performance in two multicenter trials in ophthalmology. Control Clin Trials. 1990;11:374–394. doi: 10.1016/0197-2456(90)90177-4. [DOI] [PubMed] [Google Scholar]
  • 31.Kong Q, Mei H, Lai Y, et al. Barriers and facilitators to participation in clinical trial among lymphoma patients from Sun Yat-sen University Cancer Center in China: An observation study. Medicine (Baltimore) 2017;96:e8062. doi: 10.1097/MD.0000000000008062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Logan JK, Tang C, Liao Z, et al. Analysis of factors affecting successful clinical trial enrollment in the context of three prospective, randomized, controlled trials. Int J Radiat Oncol Biol Phys. 2017;97:770–777. doi: 10.1016/j.ijrobp.2016.11.035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Metzger-Filho O, de Azambuja E, Bradbury I, et al. Analysis of regional timelines to set up a global phase III clinical trial in breast cancer: The adjuvant lapatinib and/or trastuzumab treatment optimization experience. Oncologist. 2013;18:134–140. doi: 10.1634/theoncologist.2012-0342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Peay HL, Biesecker BB, Wilfond BS, et al. Barriers and facilitators to clinical trial participation among parents of children with pediatric neuromuscular disorders. Clin Trials. 2018;15:139–148. doi: 10.1177/1740774517751118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Rick J, Clarke M, Montgomery AA, et al. Doing trials within trials: A qualitative study of stakeholder views on barriers and facilitators to the routine adoption of methodology research in clinical trials. Trials. 2018;19:481. doi: 10.1186/s13063-018-2862-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Salman A, Nguyen C, Lee YH, et al. A review of barriers to minorities’ participation in cancer clinical trials: Implications for future cancer research. J Immigr Minor Health. 2016;18:447–453. doi: 10.1007/s10903-015-0198-9. [DOI] [PubMed] [Google Scholar]
  • 37.Ali N, Lifford KJ, Carter B, et al. Barriers to uptake among high-risk individuals declining participation in lung cancer screening: A mixed methods analysis of the UK Lung Cancer Screening (UKLS) trial. BMJ Open. 2015;5:e008254. doi: 10.1136/bmjopen-2015-008254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Grill JD, Karlawish J, Elashoff D, et al. Risk disclosure and preclinical Alzheimer’s disease clinical trial enrollment. Alzheimers Dement. 2013;9:356–359.e1. doi: 10.1016/j.jalz.2012.03.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39. doi: 10.1186/s13063-018-2958-z. Hall DA, Moore C, Comella C, et al: Recruitment of patients with de novo Parkinson disease: Successful strategies in a randomized exercise clinical trial. Trials 19:630, 2018 . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Leavy B, Kwak L, Hagströmer M, et al. Evaluation and implementation of highly challenging balance training in clinical practice for people with Parkinson’s disease: Protocol for the HiBalance effectiveness-implementation trial. BMC Neurol. 2017;17:27. doi: 10.1186/s12883-017-0809-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Lebensburger JD, Sidonio RF, Debaun MR, et al. Exploring barriers and facilitators to clinical trial enrollment in the context of sickle cell anemia and hydroxyurea. Pediatr Blood Cancer. 2013;60:1333–1337. doi: 10.1002/pbc.24486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Liu H, Laba TL, Massi L, et al. Facilitators and barriers to implementation of a pragmatic clinical trial in Aboriginal health services. Med J Aust. 2015;203:24–27. doi: 10.5694/mja14.00581. [DOI] [PubMed] [Google Scholar]
  • 43.London L, Hurtado-de-Mendoza A, Song M, et al. Motivators and barriers to Latinas’ participation in clinical trials: The role of contextual factors. Contemp Clin Trials. 2015;40:74–80. doi: 10.1016/j.cct.2014.11.013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Mills N, Donovan JL, Smith M, et al. Perceptions of equipoise are crucial to trial participation: A qualitative study of men in the ProtecT study. Control Clin Trials. 2003;24:272–282. doi: 10.1016/s0197-2456(03)00020-5. [DOI] [PubMed] [Google Scholar]
  • 45.Presseau J, Mutsaers B, Al-Jaishi AA, et al. Barriers and facilitators to healthcare professional behaviour change in clinical trials using the Theoretical Domains Framework: A case study of a trial of individualized temperature-reduced haemodialysis. Trials. 2017;18:227. doi: 10.1186/s13063-017-1965-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.van de Glind EM, Vural EM, Scholten E, et al. Barriers to and facilitators of participation of older adults in a placebo-controlled randomized clinical trial. J Am Geriatr Soc. 2013;61:1421–1422. doi: 10.1111/jgs.12388. [DOI] [PubMed] [Google Scholar]
  • 47.Yevchak AM, Fick DM, McDowell J, et al. Barriers and facilitators to implementing delirium rounds in a clinical trial across three diverse hospital settings. Clin Nurs Res. 2014;23:201–215. doi: 10.1177/1054773813505321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Ritchie J, Lewis J. Qualitative Research Practice: A Guide for Social Science Students and Researchers. London: Sage; 2003. [Google Scholar]
  • 49.Tobin GA, Begley CM. Methodological rigour within a qualitative framework. J Adv Nurs. 2004;48:388–396. doi: 10.1111/j.1365-2648.2004.03207.x. [DOI] [PubMed] [Google Scholar]
  • 50.MacPhail C, Khoza N, Abler L, et al. Process guidelines for establishing intercoder reliability in qualitative studies. Qual Res. 2015;16:198–212. [Google Scholar]
  • 51.Sandelowski M. The use of quotes in qualitative research. Res Nurs Health. 1994;17:479–482. doi: 10.1002/nur.4770170611. [DOI] [PubMed] [Google Scholar]
  • 52. Riege A: Validity and reliability tests in case study research: A literature review with “hands-on” applications for each research phase. Qualitative Market Research 6:75-86, 2003.
  • 53.Mays N, Pope C. Qualitative research in health care. Assessing quality in qualitative research. BMJ. 2000;320:50–52. doi: 10.1136/bmj.320.7226.50. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Perlmutter J, Roach N, Smith ML. Involving advocates in cancer research. Semin Oncol. 2015;42:681–685. doi: 10.1053/j.seminoncol.2015.07.008. [DOI] [PubMed] [Google Scholar]
  • 55. Reference deleted.
  • 56.Cohen GI. Clinical research by community oncologists. CA Cancer J Clin. 2003;53:73–81. doi: 10.3322/canjclin.53.2.73. [DOI] [PubMed] [Google Scholar]
  • 57. O’Grady MA, Cohen SJ, Keeley PA, et al: Removing barriers to clinical research in community hospitals—The Fox Chase Cancer Center Partners experience. J Clin Oncol 25, 2007 (18_suppl; abstr 6614)
  • 58. doi: 10.1200/JOP.0824602. Making research dollars stretch for community practices. J Oncol Pract 4:81-82, 2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Chino F, Zafar SY. Financial toxicity and equitable access to clinical trials. Am Soc Clin Oncol Educ Book. 2019;39:11–18. doi: 10.1200/EDBK_100019. [DOI] [PubMed] [Google Scholar]
  • 60.Copur MS, Ramaekers R, Gönen M, et al. Impact of the National Cancer Institute Community Cancer Centers program on clinical trial and related activities at a community cancer center in rural Nebraska. J Oncol Pract. 2016;12:67–68, e44-e51. doi: 10.1200/JOP.2015.005736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Copur MS. Inadequate awareness of and participation in cancer clinical trials in the community oncology setting. Oncology (Williston Park) 2019;33:54–57. [PubMed] [Google Scholar]
  • 62.Ersek JL, Graff SL, Arena FP, et al. Critical aspects of a sustainable clinical research program in the community-based oncology practice. Am Soc Clin Oncol Educ Book. 2019;39:176–184. doi: 10.1200/EDBK_238485. [DOI] [PubMed] [Google Scholar]
  • 63.Meropol NJ, Wong YN, Albrecht T, et al. Randomized trial of a web-based intervention to address barriers to clinical trials. J Clin Oncol. 2016;34:469–478. doi: 10.1200/JCO.2015.63.2257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Umutyan A, Chiechi C, Beckett LA, et al. Overcoming barriers to cancer clinical trial accrual: Impact of a mass media campaign. Cancer. 2008;112:212–219. doi: 10.1002/cncr.23170. [DOI] [PubMed] [Google Scholar]

Articles from JCO Oncology Practice are provided here courtesy of American Society of Clinical Oncology

RESOURCES