Abstract
Objectives.
We qualitatively explored patient and clinician experiences with biomarker testing in one academic health system to identify current communication practices and unmet testing information needs.
Methods.
We conducted 1:1 in-depth interviews with 15 clinicians (i.e., nurses, oncologists, pathologists) and 12 patients diagnosed with non-small cell lung cancer between January and May 2022. Participants described experiences with biomarker testing as well as associated communication practices and needs. Interviews were audio-recorded and transcribed. Analysis was informed by the Framework Method.
Results.
Patients described challenges retaining information early in their patient journey. While patients were generally aware of biomarkers and their effect on treatment options, they expressed limited knowledge of expected time delays between testing and receiving results. Additionally, many did not know their testing results. Clinicians and patients both noted no standard education material on biomarker testing is currently available. They suggested such materials could support patient knowledge and decision-making.
Conclusions.
Communication between patients and clinicians about biomarker testing is largely delivered through verbal counseling at a time when patients may be cognitively compromised. All participants supported the idea of delivering standard, tangible education materials on biomarker testing to patients.
Practice Implications.
Education materials may enhance counseling efforts and patient knowledge.
Keywords: Non-small cell lung cancer, patient education, biomarker testing
1. Introduction
Lung cancer is the leading cause of cancer-related mortality in the United States, with the majority of cases presenting as non-small cell lung cancer (NSCLC) [1, 2]. Advancements have been made in screening, diagnosis, treatment options [3], and the rapid development and use of targeted treatments have improved clinical outcomes for patients with NSCLC [4–6]. Unlike traditional chemotherapy, targeted treatments act only on cancer cells and prevent cancer cell growth by interfering with the specific mutations or abnormalities, called “biomarkers”, which drive cancer. As targeted treatments offer several advantages over existing treatment options, and are considered the future of precision medicine, rates of biomarker testing have dramatically increased over the past decade [7].
Eligibility for targeted treatments hinge on testing biopsy tissue for biomarkers (e.g., programmed cell death ligand 1 (PDL1), epidermal growth factor receptor (EGFR), anaplastic lymphoma kinase (ALK)). Results of biomarker testing can reveal the extent to which an existing targeted treatment may be a viable option for a particular patient [8]. The typical biomarker testing process requires clinicians to access an existing or obtain a new sample of the patient’s tissue or blood. Then, the sample is sent to a specialized laboratory for analysis. Finally, the results must be shared by the lab with the treating clinician. As a result of the time required for transferring patient samples and communication, it may take multiple weeks before treatment with the most appropriate therapy for a particular patient can be initiated.
Similar to other medical decisions in the context of cancer, optimal decision making around delaying treatment initiation until biomarker test results are available is a complex process. It requires thoughtful consideration and discussion of the risk and benefit balance, factoring in the patients’ history, preferences and clinical presentation [9]. Among patients with cancer generally, high quality patient-provider communication is associated with better patient outcomes including engagement in healthcare, satisfaction, and quality of life [10]. Similar findings have also been noted among patients contending with other conditions [11, 12]. Yet, limited research has examined patient-provider communication practices and needs in the context of biomarker testing for NSCLC [13, 14]. In this study, we sought to qualitatively explore current patient and clinician experiences with biomarker testing across one large academic health system.
Our goals for the study presented in this paper were: 1) to better understand barriers to patient knowledge of biomarker testing for NSCLC, 2) to solicit perspectives on current patient-provider communication practices related to biomarker testing, nd 3) to explore the appropriateness and acceptability of a potential intervention to inform patients and enhance treatment decision-making.
2. Methods
Participant recruitment and enrollment
A convenience sample of clinicians (nurses/nurse navigators, oncologists, and pathologists) involved in the care of NSCLC patients were recruited by email from five practices affiliated with a large, regional academic medical center in Chicago, IL.
Adult patients were eligible to participate if they had a diagnosis of NSCLC and were currently receiving treatment at any practice affiliated with the participating academic health center. Those who were eligible were identified through clinician referral. A nurse navigator informed potentially eligible patients about the study; those who expressed interest were phoned by a research coordinator (RC) who provided additional information about the study and conducted a screening assessment for eligibility. Informed consent was obtained through electronic signatures documented in REDCap.
Data collection
Separate semi-structured interview guides were developed to ascertain a better understanding of current experiences with biomarker testing for NSCLC from the perspective of 1) oncologists and nurses; 2) pathologists; and 3) patients. Interview guides drew from Proctor’s implementation science theory [15]. In addition to exploring barriers to patient knowledge of biomarker testing and soliciting details about current practices, specific questions explored the acceptability and appropriateness of a potential intervention strategy: the automated distribution of educational materials about biomarker testing to patients.For example, questions explored how useful participants perceived the intervention strategy might be (appropriateness), and how they might feel about engaging with it (acceptability). Researchers used the guides to conduct formative, in-depth interviews with clinicians and patients between January and May 2022. Sample sizes were deemed sufficient for saturation of themes [16].
Audio recorded interviews, lasting approximately 45–60 minutes, were conducted remotely over a secure, web-based platform. Interviews with clinicians were led by a trained RC who was accompanied by a subject matter expert (authors CW or SK) to ensure necessary information was captured. Patient interviews were conducted by a clinical health psychologist (AR) unaffiliated with the patient’s health center or medical care. At the conclusion of each interview, clinicians and patients completed a brief demographic questionnaire. Patients also completed the Newest Vital Sign, a validated measure of health literacy designed to identify whether a participant has limited, marginal or adequate health literacy [17, 18]. Finally, following each interview, interviewers wrote memos summarizing their thoughts about the interview and key data collected. All audio recordings were transcribed by an independent transcription service for analysis purposes.
Ethical Approval
Northwestern University’s Institutional Review Board provided ethical approval for all study activities. All participants provided informed consent prior to participating in their interviews. Participants were compensated for their time.
Analysis
Analysis was informed by the Framework Method, a largely deductive approach to thematic analysis of qualitative data [19]. To begin, qualitative analysts created a list of a priori codes, drawn from the interview guides. They subsequently read a subset of transcripts for familiarity and content, wrote memos, and summarized interviews; information gained during this process resulted in a list of potential emergent codes. Together, the list of a priori and emergent codes comprised the initial codebook which was piloted on a subset of four transcripts. Iterative refinement of the codes and code definitions ensured their consistent application. Once the codebook was finalized, each transcript was double coded in NVivo by two PhD-level qualitative researchers who met regularly to achieve coding consensus; discrepancies were fully reconciled. After all transcripts were coded, separate Excel matrices for clinicians and patients were created to facilitate the identification of themes across participants and to display illustrative quotes. As described by the Framework Method, individual participants were represented in rows, while separate codes formed the basis of each column; summaries of each code were written across participants and findings revealed key themes [19, 20]. As a form of member checking, initial findings were compared with post-interview memos and also shared with interviewers and the study team for validation.
3. Results
Participant characteristics
A total of 15 clinicians provided electronic informed consent and were enrolled. Clinician participants included three nurses/nurse navigators, six oncologists and six pathologists, working in at least one of five different practices across Northwestern Medicine. Most were involved in the care of patients with NSCLC. A third (33%) were female.
A total of 12 patient participants were enrolled. Participant demographics and cancer-related history are provided in Table 1. Patient participants had a mean age of 58 (range 40–70). The majority of patient participants were treated at the urban practice (83%); the others were treated at affiliate, community sites. The majority were female (83%), and self-identified as White (83%). Employment status was varied with nearly half (42%) working, a third (33%) unable to work due to their illness, and a quarter (25%) retired. Over half (58%) had a college degree or higher. Nearly all (92%) were classified as having adequate health literacy, and nearly all (92%) reported receiving biomarker testing.
Table 1:
Participant Demographics and Cancer-Related Information
| Clinician Participants | |
|---|---|
| Characteristic | Value (N=15) n (%) |
| Female | 5 (33%) |
| Clinician type | |
| Nurse/nurse navigator | 3 (20%) |
| Oncologist | 6 (40%) |
| Pathologist | 6 (40%) |
| Practice location | |
| Central | 4 (27%) |
| Suburban | 7 (47%) |
| Rural | 1 (7%) |
| Suburban and rural | 3 (20%) |
| Patient Participants | |
| Characteristic | Value (N=12) |
| Age | |
| mean (SD) | 57.6 (9) |
| n (%) | |
| Age | |
| 40–49 | 2 (17%) |
| 50–59 | 5 (42%) |
| 60–69 | 3 (25%) |
| 70–75 | 2 (17%) |
| Female | 10 (83%) |
| Ethnicity | |
| Hispanic | 2 (17%) |
| Non-Hispanic | 10 (83%) |
| Race | |
| White | 10 (83%) |
| Asian | 2 (17%) |
| Employment Status | |
| Working for pay | 5 (42%) |
| Unable to work due to illness | 4 (33%) |
| Retired | 3 (25%) |
| Education | |
| Some college or technical school | 5 (42%) |
| College degree or higher | 7 (58%) |
| Household income | |
| $10–19,999 | 1 (8%) |
| $50–74,999 | 3 (25%) |
| $75–99,999 | 1 (8%) |
| $100,000+ | 7 (58%) |
| Location of Treatment Practice | |
| Central | 10 (83%) |
| Rural | 2 (17%) |
| Health literacy | |
| Limited | 0 (0%) |
| Marginal | 1 (8%) |
| Adequate | 11 (92%) |
| Reported biomarker testing | 11 (92%) |
Thematic findings
Themes from our analysis of qualitative data are described below according to the key questions we sought to answer: 1) What barriers exist to patient knowledge of biomarker testing for NSCLC? 2) What are current patient-provider communication practices related to NSCLC? 3) What do participants think about the standardized distribution of tangible educational materials to patients and what recommendations do they have?
1. What barriers exist to patient knowledge of biomarker testing for NSCLC?
1a. Knowledge retention early after NSCLC diagnosis can be challenging for patients.
Nearly every patient reported a sense of shock and feeling overwhelmed at the time of their diagnosis which, for some, lasted several months. One patient explained:
“I was in like a daze, going through the motions of things. I didn’t have any clue what was going on for six months until I broke out of my daze and got control.”
(Female Patient, Age 42)
Providers affirmed this general feeling from patients as well. A nurse navigator noted:
“It’s a very overwhelming time and everyone is focused on ‘When am I going to start treatment? How am I going to feel?’”
(Female Nurse Navigator, ID 6)
Participants described both an emotional period of adjustment to the diagnosis and a primary concern among patients for initiating treatment as soon as possible. Retention of cancer-related information, recall of early conversations, and decision-making were reportedly impaired for many patients.
1b. Despite a general awareness of biomarker testing and its purpose, patients lack clarity about the time necessary for processing results.
Most patients reported an awareness of biomarker testing and a general sense of its purpose. One participant recounted:
“I could be wrong, but this is how I remember. I know I have cancer. They just want to know what kind I have so they can decide what kind of medication should I [receive].”
(Female Patient, Age 75)
This patient, like many, understood biomarker testing had implications for her treatment plans. Nevertheless, most patients also revealed they were uncertain about key details. For example, most reported not knowing how long it would take to process and receive the results of their biomarker testing.
“They just said I was going to have the testing, then they called me when I got it. … I didn’t know if I was waiting longer than other people waited to get that.
(Female Patient, Age 75)
As such, the waiting period was seen by some as further contributing to their sense of feeling overwhelmed.
“I felt like oh, my God, we’re wasting this time. I had faith in my doctor, but I was worried, you know. Like, I don’t want it to spread any more… So, it was hard. You know, it was difficult.”
(Female Patient, Age 62)
Another patient further explained the difficulty in waiting, as he also was eager to start treatment:
“It’s a long, long [waiting period]. And not knowing is the worst part. And not getting any treatment.”
(Male Patient, Age 55)
2. What are current patient-provider communication practices related to NSCLC?
2a. Communication is largely verbal though patients receive the written pathology report.
Nearly all patients indicated they had received some information informing them, at or around the time diagnosis, that they were to receive biomarker testing. This information, they revealed, was largely delivered through in-person conversations with oncologists. For example, one patient noted:
“[My oncologist] explained what they were doing and what it was for, which is good because again, this is all new to me.”
(Female Patient, Age 51)
Once tests had been processed, most patients also reported receiving their results through in-person clinic visits. A majority of nurses and oncologists described similar situations, explaining that they try to meet in-person with patients to deliver biomarker testing results.
“So generally speaking, I don’t do that over the phone. They actually have to come in. I don’t release it in MyChart.”
(Male Oncologist, ID 3)
Although results were largely communicated verbally, some patients described the experience of receiving a written copy of their pathology report. These reports were nearly always coupled with counseling, yet patients explained that the tangible information they received was in “medical speak” or simply “too much” to process at that point in time. One patient described this situation, claiming:
“I mean she gave me the results and, again, I mean some of it, it’s just I’m looking at this, and it’s like, I have to look up what these words mean… It’s just, it’s like medical speak or like with lawyers, it’s just, it’s like for some reason [they’ve] got to make it more complicated than it needs to be in my opinion.”
(Male Patient, Age 50)
This patient, similar to several others, reported relying on his spouse to research the information they had difficulty understanding.
2b. No standard, plain language education material is currently given to patients.
When asked whether written materials are provided to patients to support understanding of biomarkers and/or testing results, nearly all clinicians indicated that no standard material is currently provided, though several volunteered that it would be useful to have such information. For example, an oncologist deliberated:
“When I’m doing my discussion, and even in follow-up, if I’m going over the NGS results at the follow-up visit, yeah, I don’t give them any handouts at that point. I mean, I guess that would be good. I actually never thought about it… But, yeah, it probably would be nice, something to simplify.”
(Female Oncologist, ID 9)
Another oncologist explained that he usually writes tailored after-visit summaries for patients. He reported:
“I usually type up a little after-visit summary. My after-visit summaries tend to be long. And I will tell them that because of this mutation, we’re going to do this therapy. I may give one sentence on the major side effects, but I’ll spend more time talking to them.”
(Male Oncologist, ID 3)
A couple of clinicians specified that patients are given written education materials once “they have a target and a particular drug” (Female Oncologist) identified, though “as of right now, there really isn’t any [system-wide] material [on biomarker testing]” (Female Nurse Manager). A nurse navigator spoke of providing patients with written education, though she noted she provides materials from patient advocacy organizations, as opposed to standard in-house materials.
“I know like I give [information from an advocacy group] and it’s a booklet, like what is biomarker testing. I give that to patients that are interested. But I don’t know specifically that we have anything about biomarker testing [internally]”
(Female Nurse Navigator, ID 6)
3. What do participants think about the standardized distribution of tangible educational materials to patients and what recommendations do they have?
3a. The standardized distribution of education materials was perceived as acceptable and appropriate, potentially able to support knowledge and enhance patient-provider communication.
Participants were asked their opinions about delivering education on biomarker testing to patients; all had positive reactions, perceiving the strategy to be highly acceptable. Both patients and clinicians offered suggestions for the content they deemed to be appropriate. Most commonly, participants felt it would be important to receive brief, plain language information on what biomarkers are, the rationale for conducting biomarker testing, and the length of time it typically takes to receive results. For example, one patient explained:
“I think when [my oncologist] gave us the many pages [of the pathologist report], it was pretty overwhelming. I think it would be nice to have something simple at the onset … I think instead of having the six pages of information on the biomarkers, to just have something simple.”
(Female Patient, Age 57)
This patient noted she would have found a brief, simple material more appropriate than the pathology report she received. An oncologist similarly suggested that plain language information about biomarker testing, and its purpose, would be useful when he noted:
“I think just more kind of a generic explanation about what biomarker testing is, how we use it, why we use it… it’s not any type of guarantee that we’re going to do something. But we always check it just to profile the tumor and learn more about it.”
(Male Oncologist, ID 7)
Some participants explained they would also find it useful to receive information related to the processing time for biomarker testing. For example:
“…[G]ive more specifics, like, ‘Yeah, this is going to take two weeks. But this is what we’re looking for: when this test result comes in, we’re hoping to narrow down a treatment plan for you which could entail specific targeted medications to treat your cancer.’ Anything like that I think would be helpful.”
(Male Patient, Age 55)
An estimated timeframe, in this patient’s opinion, would be an appropriate addition to information describing the purpose of biomarker testing as it could serve as rationale for delaying treatment. This was similarly suggested by a pathologist who noted that providing information about the results processing time would be useful not only to patients but also to clinicians:
“So, having that in an automated way say, sample was received in the lab at this time, expected report date would be next Friday, you know what I mean. That would be ideal, not just for our patients but for our clinicians.”
(Male Pathologist, ID 202)
3b. Less frequently mentioned suggestions for material content included providing information on cost and support resources, as well as ensuring the information is unbiased and not subject to change.
Specific suggestions were made by a subset of patients who wanted to receive information about the cost of testing and/or a list of resources with additional information or support services (e.g., testimonials from patients with shared experiences). For example, one patient noted:
“One thing that I didn’t touch on was, some of this is at your expense. Your insurance company doesn’t always cover it. I think that’s really important because my insurance company may not be paying for one of [the tests]. That’s out of pocket. Depending on your insurance, it could really be significant to some people.”
(Female Patient, Age 57)
For her, the potential out-of-pocket costs were a concern. Another patient, though, noted she would find social support from individuals with similar experiences helpful:
“If there are other people who have had experience with biomarkers, could they be kind of on a list so that the patient could actually talk to them about concerns that they have.”
(Female Patient, Age 65)
A few patients also had ideas about how to increase the trustworthiness of the information, such as using unbiased descriptions or ensuring the information is delivered by a trusted source (e.g., their physician).
From the clinician perspective, several cautioned that content should not reference details that could reasonably be expected to change over time. For example, one clinician who noted that general educational materials have “definitely been missed in [his] practice thus far,” advised:
“I wouldn’t want to get into the nitty gritty of ‘This is what [specific biomarkers are] mostly because those are ever changing, and as we have new targeted therapies, we add another one in there. I think it would be hard to manage the education with those changing like that.”
(Male Nurse Navigator, ID 5)
4. Discussion and Conclusion
4.1. Discussion
In this formative study, we sought to qualitatively explore clinician and patient experiences with biomarker testing for NSCLC at one large academic health system. Participant demographics were largely reflective of those who provide and seek care for NSCLC within the participating health system. Our thematic findings are similar to a recent mixed-methods study which revealed patients are often aware of biomarker testing, and informed about the outcomes from their doctors, but do not always understand the terms printed in their results reports [14].
Participants in our study supported the idea of providing patients with standard, plain language education materials on biomarker testing, finding the idea acceptable and appropriate. Carefully designed materials conveying relatively basic and stable information could potentially support patient knowledge and enhance patient-provider communication across a large and diverse health system [21]. Lung cancer advocacy groups have conducted patient-focused research on biomarker testing for NSCLC with similar findings, highlighting a need for clear and consistent terminology [22], as well as plain-language materials to support biomarker education and enhanced communication strategies [9, 23]. Research on health literacy has revealed the importance of avoiding jargon when communicating with patients [24]. Yet, the complex and rapidly evolving state of precision medicine [25] makes this even more important when developing education on biomarker testing. Selecting content that is unlikely to change and presenting it in a way that is easy to read is critical not only for patient understanding, but also for enhanced patient-provider communication, and ultimately, improved health outcomes [26].
Findings from our study also suggest that although participants supported the idea of patient education materials on biomarker testing, automated delivery of those materials should be considered. With clinicians struggling to maintain busy practices, educational interventions designed to have minimal impact on clinical workflow may have the greatest utility [27, 28]. Nevertheless, challenges raised by our participants included some that are not likely to be addressed through education. Future research is needed to explore how best to connect patients with NSCLC to social and/or financial support services.
This study may have limited generalizability as it included a small sample of patients receiving treatment and providers affiliated with a single academic medical center. While this health system consisted of clinics located in both urban and rural settings, these results may be different than the experiences of patients and clinicians in different health systems. Furthermore, the clinician-referral recruitment strategy of patients resulted in a largely white, well-educated sample of patients with adequate health literacy. ultural considerations may need to be explored in future research. It is also worth noting that, despite adequate health literacy, these patients still reported difficulty understanding some of the information they received.
4.2. Conclusion
Findings revealed that communication between clinicians and patients about biomarker testing is largely delivered through verbal counseling at a time when patients may have challenges retaining key information. Main challenges included a lack of understanding about the length of time necessary to receive biomarker test results, and to understand the results themselves.
4.3. Practice Implications
Results from our qualitative enquiry are currently being used to inform an intervention strategy, embedded within the electronic health record system, and designed to supplement verbal counseling on biomarker testing with written educational materials. Low literacy materials, generally describing biomarker testing and its purpose, may facilitate knowledge retention and reduce overwhelming feelings among patients newly diagnosed with NSCLC; they may also enhance patient-clinician communication. Yet, while such interventions could potentially standardize communication practices, the delivery timing and incorporation into clinical workflows will need to be carefully considered. As biomarker testing expands, results of this work could inform other similar interventions.
Highlights.
Patients had limited knowledge about when they would receive biomarker results
No standard education material on biomarker testing is routinely provided
Education materials on biomarker testing could support patient knowledge
Acknowledgements
Grant Support:
This work was supported by funding from Eli Lilly and, in part, by the National Institutes of Health’s National Institute on Aging, Grant Number P30AG059988. The opinions expressed in this paper are those of the authors and do not necessarily represent those of Eli Lilly or National Institutes of Health. REDCap software is supported by the National Institutes of Health’s National Center for Advancing Translational Sciences, Grant Number UL1TR001422. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Conflict of Interest Disclosure Statement:
Dr. Pack reports grants from RRF Foundation for Aging, Gordon and Betty Moore Foundation, Merck, Pfizer, Eli Lilly, and Gilead through her institution, and personal fees from Gilead. Dr. Bailey reports grants from the NIH, Gilead, Merck, Pfizer, Gordon and Betty Moore Foundation, RRF Foundation for Aging, Lundbeck, and Eli Lilly via her institution and personal fees from Gilead, Sanofi, Pfizer, University of Westminster, Lundbeck, and Luto UK outside the submitted work. Ms. Weldon is an employee of Executive Frameworks, Ltd who receives consulting fees from Genentech, Roche, and LUNGevity; and reports grants from Pfizer Foundation, Eli Lilly, Lung Cancer Research Foundation, and Association of Community Cancer Centers; and is a sub-awardee under UCSF’s NHGRI R01HG011792. Dr. Wolf reports grants from the NIH (NIA, NIDDK, NINR, NHLBI, NINDS), Gordon and Betty Moore Foundation, RRF Foundation for Aging and Eli Lilly, Glaxo Smith Klein, and personal fees from Pfizer, Sanofi, Luto UK, University of Westminster, and Lundbeck.
Footnotes
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CRediT authorship contribution statement
Allison Pack: Writing – Methodology, Formal analysis, Original draft preparation.
Andrea Russell: Project administration, Methodology, Investigation, Formal analysis, Writing – Reviewing and editing.
Sheetal Kircher: Investigation, Writing – Reviewing and editing.
Christine Weldon: Investigation, Writing – Reviewing and editing.
Stacy C. Bailey: Conceptualization, Writing – Reviewing and editing.
Karen Lockwood: Conceptualization, Project administration, Writing – Reviewing and editing.
Tyler Marquart: Writing – Reviewing and editing.
Ana Sofia Afonso: Writing – Reviewing and editing.
Nalin Payakachat: Writing – Reviewing and Editing.
Michael Wolf: Conceptualization, Methodology, Writing – Reviewing, Funding acquisition.
Prior Presentations: Findings will be presented in a poster for the 2023 Society of General Internal Medicine (SGIM) on May 10–13, 2023.
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