Mixed Methods Evaluation of Gaps and Barriers in Delivery of Precision Oncology in Advanced Lung Cancer

Background: Lung cancer is the leading cause of cancer mortality and has well-described disparities in outcomes. Significant survival gains in non–small cell lung cancer (NSCLC) have been achieved due to precision oncology; however, shortfalls in its delivery will further exacerbate disparities. Patient navigation is an approach to address cancer care disparities. We sought to characterize the barriers and facilitators to precision oncology through a mixed methods approach.

Methods: We performed a cross-sectional study of patient navigators, pathologists, and clinicians in North Carolina. We conducted surveys and interviews to assess barriers and facilitators to effective delivery of precision medicine for patients with advanced NSCLC, including next-generation sequencing (NGS) and use of targeted therapies and immunotherapy. We recruited both community-based and academic cancer providers across the state.

Results: Fifty-six participants completed the survey, with representation from both community and academic sites, and 5 completed interviews. Clinicians reported gaps in delivery of precision medicine as well as knowledge gaps, feeling “not at all” or “a little bit” knowledgeable about NGS (19%), liquid biopsy (32%), and targeted therapies (19%). Navigators endorsed common conversations about precision medicine but felt “somewhat” or “very” uncomfortable discussing NGS (38%), targeted therapies (31%), and had limited confidence in resolving barriers. Qualitative interviews highlighted potential solutions, including financial aid, dedicated pathology support, use of liquid biopsy, and partnership with social work.

Conclusion: Academic and community-based clinicians in North Carolina reported gaps in delivery of precision oncology in advanced NSCLC. Navigators reported a significant role in precision oncology education and delivery but limited confidence in doing so. Qualitative data highlight potential strategies for improving access. These findings suggest a need for further interventions and education to support clinicians and navigators disseminating precision oncology.

In 2023, lung cancer was the third most common cancer in the United States with more than 238,000 cases and the leading cause of cancer death with over 125,000 deaths.¹ Disparities in lung cancer are well described, with rural, underinsured, and minoritized racial and ethnic groups more likely to present with advanced disease.^2-9 Significant improvements in survival with advanced non–small cell lung cancer (NSCLC) have been achieved in recent years due to the emergence of precision oncology, which involves testing tumors or circulating cell-free DNA for molecular markers that indicate sensitivity to targeted therapies or immunotherapy.^10-16 Early data suggest disparities in the dissemination of precision oncology, with lower rates of biomarker testing and receipt of targeted therapies among patients of color, patients with Medicaid, and the underinsured.^17-19

Precision oncology is essential for the delivery of high-quality lung cancer care, but shortfalls in biomarker testing and targeted therapies will further exacerbate disparities in lung cancer survival.^19,20 Barriers to precision medicine implementation have been described, including understanding and identifying appropriate tests, interpretation of test results, and financial concerns.²¹ Patient navigation is one compelling approach to understanding and addressing barriers to equitable precision oncology. Numerous studies have demonstrated improvements in care across the cancer continuum due to patient navigation.^22-31 To ensure the benefits of precision oncology are shared among underserved populations, it is critical to understand the roles of patient navigators, pathologists, and clinicians in the delivery of precision medicine and the barriers and facilitators to equitable care.

This study sought to better characterize barriers and facilitators to precision oncology through a mixed methods approach utilizing surveys and in-depth interviews with navigators, oncology clinicians, and pathologists in North Carolina.

Methods

Design, Setting, Participants

We performed a cross-sectional study of providers in the state of North Carolina who care for patients with advanced NSCLC. We included patient navigators, pathologists, and clinicians (inclusive of oncologists and advanced practice providers), as these roles are the most directly involved in the delivery of precision medicine through ordering specific testing, prescribing therapies, and coordinating care. For this study, “navigators” refers to all patient navigators, inclusive of nurse navigators, patient navigators, and others. Our study was based at the University of North Carolina (UNC) Medical Center in Chapel Hill, a public, academic, tertiary care medical system that serves as the primary referral center for the state and has a diverse patient population in socioeconomic status, insurance, and race/ethnicity. In addition to the academic site, UNC has a network of affiliate sites that provide community oncology care. We invited oncology clinicians, pathologists, and patient navigators from UNC Medical Center and affiliate sites and elicited participation from community-based cancer centers in the area. Survey invitations were emailed directly to key contacts at the medical center, affiliate sites, and in statewide professional societies. Those contacts were also encouraged to forward the invitation within networks of cancer care providers, thus an exact number of invitations distributed could not be ascertained. Participants were invited to complete the survey, the interview, or both. Compensation was provided for participation. As patient navigators were a focus of the study, we advertised our study to all navigators at the North Carolina Oncology Navigator Association annual conference. In addition, we circulated an invitation to the survey via email to a list of known navigators in the state, maintained by the NC Cancer Hospital, constituting 249 individuals.

We developed a survey eliciting provider perceptions of demographics of the patient population served, patient understanding of precision oncology, and responsibility of care team members in delivering precision oncology.

Survey

We developed a survey eliciting provider perceptions of demographics of the patient population served, patient understanding of precision oncology, and responsibility of care team members in delivering precision oncology. We asked about each of the elements of precision medicine recommended by the National Comprehensive Cancer Network guidelines for NSCLC,³² how frequently they were discussed and ordered, as well as how knowledgeable providers felt with each. We asked about specific barriers and facilitators to delivery of care, based upon literature review.^21,33-39 Our survey was developed with an expert in survey design, piloted with several navigators and pathologists, and adapted to integrate feedback. Surveys were tailored to the specific roles of clinicians, navigators, and pathologists. Answer choices were on a 5-point Likert scale ranging from >80% of the time signifying “almost always,” 60% to 80% meaning “often,” 40% to 60% indicating “sometimes,” 20% to 40% meaning “rarely,” and <20% meaning “almost never.” Survey respondents were not required to answer every question, thus not all questions have the same number of responses.

Qualitative Interviews

An interview guide was developed with input from the qualitative research team within the North Carolina Translational and Clinical Sciences Institute (NC TraCS), a National Institutes of Health–funded, multidisciplinary resource for researchers providing expertise in several methodologies, including qualitative research. Interviews were semistructured, lasted between 30 minutes and 1 hour, and were audio-recorded and transcribed verbatim. During the interviews, we elicited information about the processes for delivering precision medicine, barriers and facilitators to care delivery, and specific challenges for particular underserved patient populations (rural, patients of color, limited socioeconomic or educational backgrounds). Our goal was to achieve thematic saturation and conduct iterative, thematic qualitative content analysis. Given the limited number of completed interviews, we instead chose to analyze our interview data utilizing rapid assessment. Thus, each interview transcript was analyzed using a summary template developed with qualitative research specialists from NC TraCS. Summary templates were then collectively synthesized into a thematic domain matrix allowing for active and expedited comparative assessment of interview data.

Statistical Analysis

Descriptive statistics were performed on survey responses. Further statistical analysis was not performed due to the small sample size.

Results

Participants

We received survey responses from 56 participants (23 patient navigators, 17 clinicians, and 16 pathologists) from January 2022 to June 2023 (Table 1). An initial 300 survey invitations were sent, but as mentioned in our methods invitations could be forwarded. We estimate an 18.7% survey response rate based on sent invitations. Nine navigators reported working in an academic setting, 6 in a community-based setting, 3 reported “other setting,” and 5 did not answer. Nine navigators were RNs, 2 were social workers, 2 were certified nursing assistants, and the remainder had “other” professional backgrounds or did not answer. Of 17 clinicians, 10 reported working in a community-based setting, 7 in an academic setting. Nine pathologists worked in an academic setting, 3 were community- based and affiliated with an academic center, 3 were community-based and unaffiliated with an academic center, and 1 did not answer. Five interviews were completed, 2 with patient navigators, 1 with a clinician, and 2 with pathologists.

Survey Results

When asked about precision medicine discussions with patients with advanced NSCLC, respondents reported that key elements of care, including next-generation sequencing (NGS) and programmed death ligand 1 (PD-L1) testing, were commonly but not universally discussed. Over half (56%) of surveyed clinicians reported almost always discussing NGS, while 13% and 6% reported rarely and almost never discussing it, respectively. Three-quarters of clinicians reported almost always discussing tumor testing for PD-L1, with only 6% almost never discussing it. Liquid biopsy was variably discussed, with 19% of clinicians almost always discussing it, but 44% almost never. Precision oncology–based treatment options were less consistently discussed in our sample. Immunotherapy was almost always discussed by 56% of clinicians, while targeted therapies were almost always discussed by 44% of clinicians but almost never by 19% (Table 2).

In terms of delivery of precision medicine, most clinicians reported ordering the key elements of testing and treatment, but knowledge gaps in testing and treatment were reported. Seven of 10 clinicians reported almost always ordering NGS, compared with 19% who almost never ordered it. Seventy-five percent of clinicians reported almost always ordering PD-L1 testing, while 13% reported almost never ordering it. Immunotherapy was always ordered by 19% of clinicians, often by 44%, sometimes by 19%, and almost never by 13%.

Regarding knowledge about precision medicine, 69% of clinicians felt very knowledgeable about NGS testing, while 12% felt somewhat knowledgeable and 19% only a little bit knowledgeable. Clinicians were very familiar with PD-L1 testing and immunotherapy, with 81% reporting feeling very knowledgeable about both. There were knowledge gaps regarding liquid biopsy, as only 56% reported feeling very knowledgeable, 19% not knowledgeable, and another 25% felt either a little bit or somewhat knowledgeable.

The most common reasons to forgo molecular or PD-L1 testing were inadequate sample (56%), risks of obtaining tissue (38%), and histology (25%). Interestingly, 25% reported omitting testing due to patient refusal, and testing was omitted due to concerns about insurance coverage (13%) or excessive cost to the patient (13%). The most frequently endorsed barrier to prescribing targeted treatment was patient comorbidities (38%), followed by patient refusal (31%), lack of clinical benefit (31%), and indeterminate results (31%). Multiple barriers could be selected by respondents, leading the total to exceed 100%. Delays in test results were reported by 25%. Cost of treatments (19%) and lack of insurance coverage (13%) were also endorsed. Clinicians largely found testing to be easy; only 7% described NGS or liquid biopsy as somewhat difficult.

Navigators variably reported discussions about precision medicine with patients with newly diagnosed, advanced NSCLC (Figure 1). Thirty-eight percent reported almost always or often discussing NGS, PD-L1 testing, and targeted therapies, and 44% almost always or often discussed immunotherapy. Only 7% reported that discussions were rare for NGS, PD-L1, or targeted therapies, 13% for liquid biopsy, and 0% for immunotherapy. However, 31% answered “not sure.” Notably, navigators endorsed frequent discomfort with these discussions and a lack of confidence in resolving barriers (Figure 2). Many were either somewhat or very uncomfortable discussing NGS (38%), PD-L1 testing (44%), liquid biopsy (44%), targeted therapies (31%), or immunotherapy (31%). Navigators were either slightly or not at all confident resolving barriers related to biomarker testing (47%) and PD-L1 testing (47%), with only slight confidence in resolving barriers to treatment with targeted therapies (47%) or immunotherapy (40%). The most common barriers to testing were insurance (endorsed by 67%), financial (56%), language (47%), communication (47%), scheduling (47%), or perceptions/beliefs (47%). Again, multiple responses were permitted.

Qualitative Interviews

While thematic saturation was not achieved given our small sample size, several interviews discussed barriers to precision medicine along with strategies and potential solutions to mitigate those barriers (presented in Table 3 with illustrative quotations). Overall, interviewees highlighted important aspects of delivering precision medicine, including the individualized nature of care: “You just have to see each patient individually, and what’s a challenge for one patient might not be for the next. You just have to specialize care for each individual patient.” One challenge was the complexity of precision medicine. A clinician noted that there are “so many changes with precision medicine, it’s hard to keep up with all the new things,” and that it can be “challenging to keep up with the evolution of knowledge on targetable mutations and medications that correspond to specific mutations.” Additional barriers identified through interviews were organized across 3 primary areas: barriers to testing, barriers to treatment, and barriers impacting specific populations.

Testing Barriers

Interviewees identified several barriers related to testing, including lack of test awareness, cost, inadequate issue sample, lack of timely results, and difficulty accessing and interpreting results. Interviewees provided possible solutions to these barriers, such as educational campaigns to bring awareness to both providers and the public, noting: “The more people hear about it, for example on television, the more they will know to ask their provider: ‘What about this? Can you do this test for me? Can you refer me somewhere they will do the test for me?’” Cost was frequently mentioned as a barrier. To address this, navigators highlighted the importance of transparency about financial assistance resources: “Just try to up-front tell them. Be honest with them and say, ‘It’s a very expensive test. However, there is some financial assistance for this, so don’t let that concern you in your decision to consent for this test…’ Just educate them on it.” To address issues of tissue sample size, interviewees suggested collaboration among proceduralists and pathologists to obtain adequate tissue, prioritize the use of molecular testing, and consider liquid biopsy. Lastly, interviewees noted that the expertise of the molecular tumor board is a solution for addressing challenges in interpreting test results: “Sometimes, there’s a different mutation that we haven’t seen before or [...] doesn’t make sense or whatever. Then that’s when they get the molecular tumor board involved.”

Treatment Barriers

Interviewees identified 4 primary barriers related to precision medicine treatment: delays in accessing molecular testing results, treatment cost, access to treatment, and patient comorbidities necessitating standard of care treatments. Interviewees noted that one way to mitigate delays to treatment stemming from a lack of access to molecular test results is to revert to standard of care treatments until test results become available. Solutions proposed to address barriers related to cost included manufacturer assistance programs, pharmacy technicians assisting with prior approvals, and use of financial navigators or social workers to assist patients facing financial challenges. One interviewee noted: “A lot of the drug companies do have manufacturers’ assistance programs for the patients. Not all of them, but a lot of them.” Interviewees noted that access to treatment can be a barrier as many precision medicine medications are only available through specialty pharmacies. To address this, interviewees proposed an electronic process for specialty pharmacy renewal and educating patients ahead of time to avoid delays: “We try to be up-front and say, ‘Don’t wait ’til you have your last pill to get a refill. Give yourself 2 weeks,’ or whatever. We try to educate them to prevent this from happening.”

Barriers of Specific Populations

Interviews identified barriers impacting specific patient groups or populations alongside potential solutions to help mitigate those challenges. Importantly, providers noted that one way to work toward equitable care is to provide universal social need screening for all patients: “I always go through the list with them and ask them: ‘Do you have any times when you don’t have money for food, for prescriptions? Are you living in your car? Are you safe at home?’ All the questions, I go over with every patient. I don’t care if they’re a state senator or if they’re a homeless person. I’m gonna ask them the same questions. You cannot make an assumption.” Specifically, to assist uninsured patients, interviewees suggested the use of manufacturer assistance, institutional charity care programs, and social workers. Interviewees also mentioned challenges related to mistrust of the medical community among Black patients, noting “sometimes patients still have the thought process of Tuskegee; they’re being experimented on.” To address these barriers, interviewees suggested educating patients on the federal approval process for cancer treatments and empowering patients to seek a second opinion if desired.

Discussion

These results offer several important findings regarding the delivery of precision medicine in advanced NSCLC. First, our respondents reported moderately high rates of uptake of key elements of precision medicine, particularly PD-L1 testing and NGS. Clinicians felt knowledgeable about NGS, PD-L1 testing, and immunotherapy and had frequent discussions with patients about these elements of care. Pathologists endorsed that biomarker testing was generally easy and did not pose a substantial burden to perform. Reference lab results were universally integrated into the electronic health record in our sample, facilitating access for clinicians and enabling results to inform treatment decisions. Navigators often had discussions with patients about precision medicine, emphasizing the important role they play in patient education and access to recommended cancer care.

However, we also observed notable gaps in uptake of precision medicine. As our survey was limited to care for patients with advanced NSCLC, national guidelines are quite clear that PD-L1 testing and NGS are standard of care. Yet nearly 20% of providers discussed NGS either rarely or not at all. Furthermore, 19% and 13% reported almost never ordering NGS or PD-L1 testing, respectively, which would suggest a practice gap in recommended care for a sizable proportion of patients. Knowledge gaps were also noted, with 19% of clinicians feeling only a little bit knowledgeable about NGS, despite this being a key standard of care for advanced NSCLC. Liquid biopsy also emerged in our results as an area with limited uptake and knowledge. While it is not universally recommended like PD-L1, peripheral blood sequencing has a growing role in improving delivery of precision medicine for patients in whom tissue biopsy is either unsafe or technically infeasible. Yet almost half of clinicians felt less than “very knowledgeable,” and more than half almost never ordered liquid biopsy despite frequently reported challenges with tissue specimen adequacy or risks of biopsy.

In addition, our findings offer insight into the active role that navigators play in the delivery of precision medicine while suggesting they may not feel adequately equipped to do so. Our surveyed navigators were mostly nurse navigators but also comprised those with social work backgrounds and patient navigators, reflecting the diversity of navigators in cancer care. Almost half of navigators reported having discussions about precision medicine testing and treatment, yet across topics, 30% to 40% of navigators did not feel comfortable with the discussions or confident in addressing barriers that might arise. These results point to a need to better educate, train, and support navigators for the complex challenges of delivering precision medicine.

A new guideline from the National Lung Cancer Roundtable offers additional guidance to acquire adequate tissue to facilitate comprehensive biomarker testing, consistent with our interview results.

The barriers identified in both the survey and the interviews are informative and provide rich context that is consistent with previous work in this field.⁴⁰ The proposed solutions described in the interviews add helpful guidance to frontline clinical providers and health system leaders on avenues for improvement. Collaborations between pathologists, proceduralists, and clinicians to guide tissue sampling approaches and testing pathways were mentioned by several individuals. Reflexive testing strategies have been described elsewhere⁴¹ and shown to be feasible, possibly expanding access to targeted therapies.^42,43 A new guideline from the National Lung Cancer Roundtable offers additional guidance to acquire adequate tissue to facilitate comprehensive biomarker testing,⁴⁴ consistent with our interview results. As noted above, education and increased utilization of liquid biopsy could also serve as a solution to the barrier of inadequate tissue or risks of biopsy, and recent work has highlighted equitable approaches to implementation.⁴⁵ Molecular tumor boards were highlighted as a strategy to address complex cases and result interpretation, again an approach with supporting evidence.46 Proposed solutions regarding use of financial assistance programs, social work, and pharmacy technicians may all assist with the cost and insurance burdens of precision medicine and will likely be helpful for patient navigators working with patients in academic and community practice alike.

Lastly, frequent barriers regarding communication, beliefs, and misconceptions emphasize the critical role that navigators can play in educating patients about the role of precision medicine in their care. The quotations about patients not understanding how medications work to control cancer or about medical mistrust by patients of color highlight the potential for navigators to improve disparities in care. Navigation has previously been shown to reduce racial disparities in lung cancer care through the innovative Accountability for Cancer Care through Undoing Racism and Equity protocol.^47,48 Use of a navigator combined with a real-time warning system that identified patients missing recommended elements of care for early- stage lung cancer was shown to eliminate the racial gap in delivery of potentially curative surgery or definitive radiation, as well as improve time to surgery.⁴⁹ This approach has been proposed as a strategy to improve care delivery and disparities in precision medicine.⁵⁰ The range of barriers identified in our study, the frequency with which navigators are already involved in precision medicine, combined with the lack of confidence and comfort navigators have with these topics reinforce that a targeted, navigation-based intervention may be well suited to improve outcomes in this field.

Limitations

Due to the concurrent pandemic and resulting strains on the cancer care and health systems, we had a low survey response rate and were not able to achieve our desired sample size in this study. That precluded statistical testing to compare responses between clinicians, navigators, or pathologists. The small number of interviews prevented us from achieving thematic saturation and thus limit the generalizability of our findings. Our findings are hypothesis generating and add context to previously published work on barriers to precision oncology. As a voluntary survey, the results may have selection bias, those who were interested and engaged in precision medicine may have chosen to respond, or those who are frustrated by it and wanted to report their challenges. However, our small sample size does still offer a diverse range of voices, evenly distributed across professions (navigators, clinicians, pathologists) and community and academic contexts.

Conclusion

In a small sample of navigators, clinicians, and pathologists, we found that precision medicine had broad uptake in key elements of testing and treatment, yet notable gaps remain in NGS and liquid biopsy testing. Navigators report a significant role in education about precision oncology but very limited comfort level in doing so, or in resolving barriers. Qualitative data highlight several potential strategies for improving access. These findings suggest a need for further interventions and education to support clinicians and navigators disseminating precision oncology in advanced NSCLC.

Funding: Fellows Grant through the NC Lung Cancer Initiative, National Center for Advancing Translational Sciences (NCATS).

The project described was supported by NCATS, National Institutes of Health (NIH), through Grant Award Number UM1TR004406. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

Conflicts of Interest: None

References

1. Common Cancer Sites—Cancer Stat Facts. Accessed December 28, 2023. https://seer.cancer.gov/statfacts/html/common.html
2. Bach PB, Cramer LD, Warren JL, Begg CB. Racial differences in the treatment of early-stage lung cancer. N Engl J Med. 1999;341:1198-1205.
3. Wolf A, Alpert N, Tran BV, et al. Persistence of racial disparities in early-stage lung cancer treatment. J Thorac Cardiovasc Surg. 2019;157:1670-1679.e4.
4. Smedley BD, Stith AY, Nelson AR. Unequal Treatment: Confronting Racial and Ethnic Disparities in Health Care. National Academies Press; 2003. doi:10.17226/12875
5. Cancer Statistics Review, 1975-2017 - SEER Statistics. Accessed August 25, 2020. https://seer.cancer.gov/csr/1975_2017/
6. Nicoli CD, Sprague BL, Anker CJ, Lester-Coll NH. Association of rurality with survival and guidelines-concordant management in early-stage non-small cell lung cancer. Am J Clin Oncol. 2019;42:607-614.
7. Atkins GT, Kim T, Munson J. Residence in rural areas of the United States and lung cancer mortality. disease incidence, treatment disparities, and stage-specific survival. Ann Am Thorac Soc. 2017;14:403-411.
8. Niu X, Roche LM, Pawlish KS, Henry KA. Cancer survival disparities by health insurance status. Cancer Med. 2013;2:403-411.
9. Ellis L, Canchola AJ, Spiegel D, et al. Trends in cancer survival by health insurance status in California from 1997 to 2014. JAMA Oncol. 2018;4:317-323.
10. Yang S-R, Schultheis AM, Yu H, et al. Precision medicine in non-small cell lung cancer: current applications and future directions. Semin Cancer Biol. 2022;84:184-198.
11. Vargas AJ, Harris CC. Biomarker development in the precision medicine era: lung cancer as a case study. Nat Rev Cancer. 2016;16:525-537.
12. Singh A, Chen H. Optimal care for patients with anaplastic lymphoma kinase (ALK)-positive non-small cell lung cancer: a review on the role and utility of ALK inhibitors. Cancer Manag Res. 2020;12:6615-6628.
13. Kris MG, Johnson BE, Berry LD, et al. Using multiplexed assays of oncogenic drivers in lung cancers to select targeted drugs. JAMA. 2014;311:1998-2006.
14. Steuer CE, Behera M, Berry L, et al. Role of race in oncogenic driver prevalence and outcomes in lung adenocarcinoma: results from the Lung Cancer Mutation Consortium. Cancer. 2016;122:766-772.
15. Barlesi F, Mazieres J, Merlio J-P, et al. Routine molecular profiling of patients with advanced non-small-cell lung cancer: results of a 1-year nationwide programme of the French Cooperative Thoracic Intergroup (IFCT). Lancet. 2016;387:1415-1426.
16. Howlader N, Forjaz G, Mooradian MJ, et al. The effect of advances in lung-cancer treatment on population mortality. N Engl J Med. 2020;383:640-649.
17. Kehl KL, Lathan CS, Johnson BE, Schrag D. Race, poverty, and initial implementation of precision medicine for lung cancer. J Natl Cancer Inst. 2019;111:431-434.
18. Lynch JA, Berse B, Rabb M, et al. Underutilization and disparities in access to EGFR testing among Medicare patients with lung cancer from 2010 - 2013. BMC Cancer. 2018;18:306.
19. Palazzo LL, Sheehan DF, Tramontano AC, Kong CY. Disparities and trends in genetic testing and erlotinib treatment among metastatic non-small cell lung cancer patients. Cancer Epidemiol Biomarkers Prev. 2019;28:926-934.
20. Masters GA, Temin S, Azzoli CG, et al. Systemic therapy for stage IV non-small-cell lung cancer: American Society of Clinical Oncology Clinical Practice Guideline Update. J Clin Oncol. 2015;33:3488-3515.
21. Ersek JL, Black LJ, Thompson MA, Kim ES. Implementing precision medicine programs and clinical trials in the community-based oncology practice: barriers and best practices. Am Soc Clin Oncol Educ Book. 2018;38:188-196.
22. Battaglia TA, Bak SM, Heeren T, et al. Boston Patient Navigation Research Program: the impact of navigation on time to diagnostic resolution after abnormal cancer screening. Cancer Epidemiol Biomarkers Prev. 2012;21:1645-1654.
23. Paskett ED, Katz ML, Post DM, et al. The Ohio Patient Navigation Research Program: does the American Cancer Society patient navigation model improve time to resolution in patients with abnormal screening tests? Cancer Epidemiol Biomarkers Prev. 2012;21:1620-1628.
24. Raich PC, Whitley EM, Thorland W, et al. Denver Patient Navigation Research Program. Patient navigation improves cancer diagnostic resolution: an individually randomized clinical trial in an underserved population. Cancer Epidemiol Biomarkers Prev. 2012;21:1629-1638.
25. Charlot M, Santana MC, Chen CA, et al. Impact of patient and navigator race and language concordance on care after cancer screening abnormalities. Cancer. 2015;121:1477-1483.
26. Valverde PA, Calhoun E, Esparza A, et al. The early dissemination of patient navigation interventions: results of a respondent-driven sample survey. Transl Behav Med. 2018;8:456-467.
27. Cantril C, Haylock PJ. Patient navigation in the oncology care setting. Semin Oncol Nurs. 2013;29:76-90.
28. Wells KJ, Winters PC, Jean-Pierre P, et al. Effect of patient navigation on satisfaction with cancer-related care. Support Care Cancer. 2016;24:1729-1753.
29. Neal CD, Weaver DT, Raphel TJ, et al. Patient navigation to improve cancer screening in underserved populations: reported experiences, opportunities, and challenges. J Am Coll Radiol. 2018;15:1565-1572.
30. Simon MA, Trosman JR, Rapkin B, et al. Systematic patient navigation strategies to scale breast cancer disparity reduction by improved cancer prevention and care delivery processes. JCO Oncology Practice. 2020;16:e1462-e1470.
31. Paskett ED, Harrop JP, Wells KJ. Patient navigation: an update on the state of the science. CA Cancer J Clin. 2011;61:237-249.
32. Ettinger DS, Wood DE, Aisner DL, et al. Non-Small Cell Lung Cancer, Version 3.2022, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2022;20:497-530.
33. Nadauld LD, Ford JM, Pritchard D, Brown T. Strategies for clinical implementation: precision oncology at three distinct institutions. Health Aff (Millwood). 2018;37:751-756.
34. Wright S, Daker-White G, Newman W, Payne K. Understanding barriers to the introduction of precision medicines in non-small cell lung cancer: a qualitative interview protocol. Wellcome Open Res. 2018;3:24.
35. Matthew DB. Two threats to precision medicine equity. Ethn Dis. 2019;29(suppl 3):629-640.
36. Levit LA, Kim ES, McAneny BL, et al. Implementing precision medicine in community-based oncology programs: three models. J Oncol Pract. 2019;15:325-329.
37. Giusti K, Young AQ, Lehrhaupt K. Closing knowledge gaps to optimize patient outcomes and advance precision medicine. Cancer J. 2018;24:144-151.
38. Ciardiello F, Adams R, Tabernero J, et al. Awareness, understanding, and adoption of precision medicine to deliver personalized treatment for patients with cancer: a multinational survey comparison of physicians and patients. Oncologist. 2016;21:292-300.
39. Whitcomb DC. Barriers and research priorities for implementing precision medicine. Pancreas. 2019;48:1246-1249.
40. Cooper KE, Abdallah KE, Angove RSM, et al. Navigating access to cancer care: identifying barriers to precision cancer medicine. Ethn Dis. 2022;32:39-48.
41. Gregg JP, Li T, Yoneda KY. Molecular testing strategies in non-small cell lung cancer: optimizing the diagnostic journey. Transl Lung Cancer Res. 2019;8:286-301.
42. Zacharias M, Absenger G, Kashofer K, et al. Reflex testing in non-small cell lung carcinoma using DNA- and RNA-based next-generation sequencing —a single-center experience. Transl Lung Cancer Res. 2021;10:4221-4234.
43. Miller TE, Yang M, Bajor D, et al. Clinical utility of reflex testing using focused next-generation sequencing for management of patients with advanced lung adenocarcinoma. J Clin Pathol. 2018;71:1108-1115.
44. Fox AH, Nishino M, Osarogiagbon RU, et al. Acquiring tissue for advanced lung cancer diagnosis and comprehensive biomarker testing: a National Lung Cancer Roundtable best-practice guide. CA Cancer J Clin. 2023;73:358-375.
45. Febbo PG, Allo M, Alme EB, et al. Recommendations for the equitable and widespread implementation of liquid biopsy for cancer care. JCO Precis Oncol. 2024;8:e2300382.
46. Huang B, Chen Q, Allison D, et al. Molecular tumor board review and improved overall survival in non-small-cell lung cancer. JCO Precis Oncol. 2021;5:1530-1539.
47. Cykert S, Eng E, Manning MA, et al. A Multi-faceted intervention aimed at Black-White disparities in the treatment of early stage cancers: the ACCURE Pragmatic Quality Improvement trial. J Natl Med Assoc. 2020;112:468-477.
48. Cykert S, Eng E, Walker P, et al. A system-based intervention to reduce Black-White disparities in the treatment of early stage lung cancer: a pragmatic trial at five cancer centers. Cancer Med. 2019;8:1095-1102.
49. Charlot M, Stein JN, Damone E, et al. Effect of an antiracism intervention on racial disparities in time to lung cancer surgery. J Clin Oncol. 2022; 40:1755-1762.
50. Stein JN, Charlot M, Cykert S. Building toward antiracist cancer research and practice: the case of precision medicine. JCO Oncol Pract. 2021;17:273-277.