Abstract
Introduction
Progress in acute lymphoblastic leukemia (ALL) affecting adolescents and young adults (AYAs), aged 15-39 years, has been challenged by aggressive disease biology, low clinical trial participation, unique supportive care needs, and heterogeneity across treatment settings with lack of age-based standardized therapy. In 2012, the National Comprehensive Cancer Network (NCCN) first issued AYA ALL treatment guidelines. In the absence of formal evaluation of the 2012 NCCN guidelines on the delivery of guideline-concordant care at National Cancer Institute (NCI) Community Oncology Research Program (NCORP) practices, we conducted a qualitative study, as part of the Children’s Oncology Group-led cancer care delivery trial ACCL16N1CD.
Methods
Structured focus groups, moderated by study members, were convened to identify barriers and facilitators to NCCN guideline-concordant treatment delivery and documentation. Healthcare professionals at NCORP sites that activated ACCL16N1CD were invited to participate if they were involved in AYA ALL care. Nine focus groups were held with 55 participants. Nominal group technique was used to rank statements about delivery and documentation. Qualitative data were analyzed using directed content analysis methodology to describe facilitators and barriers and assess emerging themes.
Results
Five main themes were identified for delivery (Care Model, Care Organization, Supportive Care, Therapeutic Approach, Individual Factors [patient; provider]) and six for documentation (Care Model, Hospital Type, Care Organization, Supportive Care, Therapeutic Approach, Individual Factors) of NCCN-concordant treatment. Supportive Care was ranked first for delivery of guideline-concordant care and Care Organization was ranked first for documentation, with Individual Factors ranking close behind for both. Theme ranking varied by focus group type and professional roles of participants.
Conclusion
Identified barriers and facilitators impacting guideline-concordant care of AYA ALL across NCORPs were aligned with institutional supportive care resources, care organization for AYA, and individual factors. Top ranked statements may be utilized as implementation strategies in future care delivery trials.
Keywords: adolescent and young adult (AYA), acute lymphoblastic leukemia (ALL), guideline concordant care, treatment guidelines, pediatric-inspired therapy
Plain Language Summary
In recent decades, adolescent and young adults (AYA) with acute leukemia have not experienced the same gains in treatment tolerance and survival compared to younger children and older adults. Specific guidelines have been developed for AYA acute leukemia treatment, yet many of these patients do not receive guideline-based therapy, particularly in community settings where most receive cancer care. This study includes a series of focus groups, held to discuss directly with community healthcare professionals who care for AYA with leukemia, what specific challenges and aids influence whether or not AYA with leukemia are able to receive guideline-based therapy in their settings. From these discussions, key factors that influence the ability to deliver therapy that is guideline-based include having supportive care resources in place for these patients, having or lacking organization of the care, and some challenges at the level of the patient or provider that may influence the care that is delivered.
1. Introduction
Survival among individuals diagnosed with acute lymphoblastic leukemia (ALL) between age 15 to 39 years (AYAs: adolescents and young adults) lags behind those diagnosed as children.1-7 Differential outcomes between AYAs and children with ALL are partly attributed to aggressive disease biology and differences in management. 8 Most AYAs with ALL are treated in community settings in increasing proportions as they age.9-11 Thus, it is essential to characterize delivery of cancer care in addition to clinical and biological aspects of AYA ALL.
As AYA ALL survival is associated with clinical trial enrollment and treatment approach, 12 the National Cancer Institute (NCI) has prioritized work in AYA cancer and clinical trial enrollment; nevertheless, AYAs remain under-represented.13-15 To address ALL outcome disparities, the National Comprehensive Cancer Network (NCCN) established clinical practice guidelines for AYA in 2012. Given superior AYA ALL outcomes with pediatric rather than adult regimens,16-21 NCCN incorporated age-specific treatment into ALL guidelines (e.g., AYA [15-39 years] vs. adults ≥40 years). 22 AYA ALL guidelines remained consistent from 2012 to 2016,22,23 recommending pediatric-inspired therapy or clinical trial enrollment for AYA with Philadelphia chromosome negative (Ph-neg) ALL (T-cell or B-cell). For Philadelphia chromosome positive (Ph-pos) ALL, guidelines recommended multi-agent chemotherapy with a tyrosine kinase inhibitor.
Given most AYA with ALL are treated in their community, the NCI Community Oncology Research Program (NCORP) is the ideal setting to examine care delivery for this population. The NCORP network includes stand-alone children’s hospitals, adult-only hospitals, and general hospitals with embedded pediatrics (i.e., mixed) across the United States (US), aiming to improve cancer research and trial access for patients closer to home.24-28 Understanding that evidence-based system-, provider- and patient-level factors contribute to AYA cancer disparities (Figure 1),1-15,29 the ACCL16N1CD study examined guideline-concordant care (GCC; specifically, NCCN guidelines) among AYA with ALL across the NCORP. Characteristics of healthcare settings where AYA with ALL receive care have been described. 30 Here we present qualitative study findings evaluating the ACCL16N1CD objective to identify for AYAs with ALL, targetable structure- and process-level barriers and facilitators that will increase the proportion of patients having a documented treatment plan and receiving treatment according to NCCN guidelines.
Figure 1.
Adolescent young adult (AYA) cancer care delivery model (Wolfson J and Bhatia S)
2. Methods
ACCL16N1CD (NCT03204916) was a retrospective, multi-center intergroup study for the NCI Cancer Care Delivery Research (CCDR) program implemented at NCORPs27,28,31 and led by the Children’s Oncology Group (COG) in collaboration with adult-focused NCORP Research Bases (Alliance for Clinical Trials in Oncology [Alliance], ECOG-ACRIN Cancer Research Group [ECOG-ACRIN], SWOG Cancer Network [SWOG]).
2.1. Institutional Participation
Institutional eligibility for ACCL16N1CD included (a) willingness to participate in all study aims, (b) classification as an NCORP between December 2017 and April 2022, and (c) treatment of ≥1 patient 15-39 years of age with B- or T-cell ALL between 2012 and 2016, regardless of clinical trial participation.
2.2. Focus Group Recruitment
Healthcare professionals at participating NCORPs caring for AYA ALL were eligible for focus groups (FGs), including (but not limited to) physicians, nurses, social workers, pharmacists, and clinical research associates; trainees were ineligible. NCORP leadership and/or research staff distributed standardized electronic invitations to eligible individuals (Appendix I); interested volunteers completed an electronic questionnaire providing role/training details regarding the location at which they delivered care (clinical facility [CF]: study-defined entity 30 ; Appendix II). The study team selected FG participants from the volunteer pool for representativeness by CF model (pediatric-only, adult-only, or mixed), academic status, NCORP classification (community vs. minority-underserved), 26 geography (US region and rural vs. urban), oncology specialty (pediatric vs. adult), and professional role. Separate FGs were conducted with physicians and non-physicians to avoid potential response censoring and bias based on hierarchical relationships, plus mixed physician/non-physician FGs to elicit new ideas. More than one individual from each NCORP could participate. Volunteer selection occurred selectively in a rolling fashion as focus groups sessions were filled. For example, for non-physician focus groups, volunteers available for a specific session were selected to account for variability across facility model first, followed by professional role, and then the remaining factors as listed above (academic status, NCORP classification, etc.).
2.3. Data Collection
FGs of 5-8 participants lasting 1.5-4 hours each were held either in person or virtually (due to COVID-19 travel limitations); in-person FGs were held, where possible, adjacent to professional meetings, and virtual FGs used Zoom video conferencing. FG sessions included volunteer participants, research team members, and COG operations staff. FGs were recorded and professionally transcribed, with thematic notes following the moderator guide (Appendix III) taken to augment the analysis; transcripts were not returned to participants. All data collection and analyses were conducted by study team members who received the same methodological training, including focus group facilitator training with the Public Health Institute’s Survey Research Group (ACG, CLK, KMB, JAW, MPB, KBB, JML, MS, WLW). FG research team members were female and included oncology clinician scientists and research nurses who did not have a prior relationship established with volunteer participants.
Nominal group technique (NGT) was used as a structured discussion method, enabling inclusive group brainstorming and prioritization of ideas for consensus that limits potential dominating perspectives.32,33 Per NGT procedures, the group first reviewed a brief background on NCCN guidelines for AYA ALL and the FG questions, specifically: (a) barriers to delivering GCC, (b) facilitators to delivering GCC, (c) barriers to documenting GCC, and (d) facilitators to documenting GCC. Participants next generated ideas independently, then presented in turn to the group at large until no new ideas were generated. Ideas were discussed for clarification and recorded by the facilitator. Participants then rank-voted all ideas twice, before and after a group discussion. In-person participants had 15 votes per round that could be allocated across ideas in any quantity to represent a weighted rank. For virtual FGs, ranking was done electronically using the Poll Everywhere® platform. The final ranked statements resulted from the sum of second-round votes received in-person or the actual ranking on the electronic platform. This process was repeated for each FG question. FGs were conducted until thematic saturation was achieved with no new themes emerging.
2.4. Analysis
Qualitative data, consisting of ranked statements generated by participants describing barriers and facilitators to GCC, were analyzed using directed content analysis with an assessment of emerging themes (Dedoose Version 9.2.012 [Computer Software]. Los Angeles, CA: SocioCultural Research Consultants, LLC. www.dedoose.com.). 34 A codebook was developed based on structure- and process-level categories from the conceptual model of AYA cancer care disparities (Figure 1; Appendix IV). 29 Seeking thematic commonality, emerging concepts that did not fall within these categories were added. Two study team members conducted independent coding (ACG, CLK) and reviewed results with two additional study team members (JAW, KMB) for consensus. The reporting of this study conforms to the COREQ guidelines. The study was approved by the NCI Pediatric Central Institutional Review Board (IRB) on September 1, 2017. Documentation of consent requirement was waived given the nature of the study. This study was conducted in accordance with the Helsinki Declaration of 1975, as revised in 2024.
3. Results
3.1. Participants
Among 167 volunteers, n=158 were eligible and n=55 were selected and participated in nine FGs (Table 1). Most participants were female (80%) and physicians (53%). Nurses represented 46% of non-physicians and 22% of all participants. Participants represented 31 CFs (Appendix VI) spanning adult (15%), pediatric (31%), and mixed (54%) CFs, with more from community practices (58%) than academic institutions (31%) or NCI-designated Comprehensive Cancer Centers (9%). Few (11%) worked in rural settings. (Details provided in Appendix VII).
Table 1.
Characteristics of Focus Group Participants: Self-Report
| | Total | § Mixed | § Non-physician | § Physician |
|---|---|---|---|---|
| N=55 (%) | Groups 1 and 3 n=14 (%) | Groups 2 and 4 n=18 (%) | Groups 5 and 6 n=23 (%) | |
| Sex | ||||
| Male | 11 (20) | 3 (21) | 0 (0) | 8 (35) |
| Female | 44 (80) | 11 (79) | 18 (100) | 15(65) |
| Profession | ||||
| Physician | 29 (53) | 6 (43) | 0 (0) | 23 (100) |
| Non-Physician | 26 (47) | 8 (57) | 18 (100) | 0 (0) |
| Registered Nurse | 12 | 5 | 7 | -- |
| Social Worker | 4 | 2 | 2 | -- |
| Psychologist | 1 | 0 | 1 | -- |
| Pharmacist | 1 | 0 | 1 | -- |
| Nurse Practitioner | 2 | 0 | 2 | -- |
| Clinical Research Associate | 5 | 1 | 4 | -- |
| Other | 1 | 0 | 1 | -- |
| Institution Type | ||||
| Adult | 8 (15) | 1 (7) | 5 (28) | 2 (9) |
| Pediatric | 17 (31) | 5 (36) | 5 (28) | 7 (30) |
| Mixed | 30 (54) | 8 (57) | 8 (44) | 14 (61) |
| Practice Setting | ||||
| Academic program | 17 (31) | 3 (21) | 8 (44) | 6 (26) |
| Community oncology program | 32 (58) | 9 (65) | 7 (39) | 16 (70) |
| NCI-designated comprehensive cancer center | 5 (9) | 2 (14) | 2 (11) | 1 (4) |
| Unknown | 1 (2) | 0 (0) | 1 (6) | 0 (0) |
| Practice Location | ||||
| Urban | 49 (89) | 13 (93) | 17 (94) | 19 (83) |
| Rural | 6 (11) | 1 (7) | 1 (6) | 4 (17) |
| Number of AYA Treated per Year | ||||
| <5 | 5 (9) | 1 (7) | 2 (11) | 2 (9) |
| 5-10 | 13 (24) | 3 (21) | 1 (6) | 9 (39) |
| 10-25 | 22 (40) | 6 (43) | 10 (56) | 6 (26) |
| >25 | 13 (24) | 4 (29) | 3 (17) | 6 (26) |
| Unknown | 2 (4) | 0 (0) | 2 (11) | 0 (0) |
| Number of ALL Treated per Year | ||||
| <5 | 9 (16) | 4 (29) | 2 (11) | 3 (13) |
| 5-10 | 9 (16) | 1 (7) | 3 (17) | 5 (22) |
| 10-25 | 17 (31) | 4 (29) | 4 (22) | 9 (39) |
| >25 | 18 (33) | 5 (36) | 7 (39) | 6 (26) |
| Unknown | 2 (4) | 0 (0) | 2 (11) | 0 (0) |
§Focus groups were comprised of either (a) only physicians, (b) only non-physicians, or (c) both physicians and non-physicians (mixed). Abbreviations: National Cancer Institute (NCI), Adolescent and Young Adult (AYA), Acute Lymphoblastic Leukemia (ALL).
3.2. Themes
The highest ranked statements from each FG are presented in Table 2. Frequencies of coded themes and sub-themes are illustrated in Figure 2; for each theme, facilitator and barrier statements were combined given their overlapping nature. For example, one group posed leadership support as a facilitator, while another group posed lack of leadership support as a barrier; both statements are coded under the same theme. A comprehensive table of coded ranked statements is in Appendix V.
Table 2.
Top Five Ranked Statements by Year and Focus Group Type
| Rank | A. Barriers to delivery | |||||
|---|---|---|---|---|---|---|
| 2019 | 2021 | |||||
| Group 1 Mixed |
Group 2 Non-physician only |
Group 3 Mixed |
Group 4 Non-physician Only |
Group 5 Physician only |
Group 6 Physician Only |
|
| 1 | Inability to give subsequent therapies due to treatment toxicity/AEs of drugs/infection. | Coordinating treatment with patient schedules as AYAs have work, families, and are less flexible. | Poor adherence to medications/appointments. | Compliance of this age group (taking medications, reporting side effects, waiting until very sick before asking for help). | Limitation/knowledge gap in local community-based providers leads to reduced cancer center referrals for ALL; provider-dependent. | Complexity of care for patient population presents challenges in getting patients easily in and out of clinic. |
| 2 | AYA referral process/source (adult PCP to adult oncology vs. pediatric PCP to pediatric oncology); inconsistent placement of patient. | Concerns about patient compliance. | AYAs are underinsured or have no insurance, also lower socioeconomic status. | Financial issues and lack of support interferes with care, ability to take time off, transportation, etc. | Age restrictions: younger AYA treated at pediatric site vs. older AYA treated at adult site with varying care/access/assessment. | Insurance status dictates location of care in some cases and drug coverage. |
| 3 | Increased adherence issues in AYA (e.g., medications). | Complexity of protocols/publications without adequate guidance. | Low clinical trial access/availability for AYA (especially in COG or non-COG sites). | Poor health literacy impacts information provided explaining treatment, understandable language, fertility issues in this age group. | Training deficiencies in pediatric-inspired regimens for adult oncology related to rarity of disease/reduced exposure to ALL leads to gap in knowledge (need for workshop, CE). | Institutional restrictions on age limitations that can be seen at certain locations. |
| 4 | Social and cultural issues impact treatment decisions (including geographic/travel challenge). | Higher cumulative doses in pediatric protocol, concern for increased toxicities. | Poor communication between pediatric and adult providers and community providers. | Determination of where a particular AYA will “fit in” for treatment (pediatric vs. adult). | Socioeconomic discrepancies. | Some subspecialists won’t see patients over age 18 at stand-alone children’s hospital. |
| 5 | Complexity of AYA pediatric backbone protocols. | Institutional resources, more is needed for pediatric regimens. | Transition to age of majority on therapy leads to challenges with buy-in/consent/adherence. | Gap in research studies available for AYA population, may not be eligible for clinical trial based on age. | Challenges in obtaining preferred laboratory/molecular sequencing assessments (including requiring case-by-case authorization). | Social workers, navigators and support staff may be less familiar with AYA specific needs/resources. |
Statements were made by focus group participants then clarified and edited using the nominal group technique approach. Abbreviations: Electronic Medical Record (EMR), Clinical Research Assistant (CRA), Registered Nurse (RN), National Comprehensive Cancer Network (NCCN) Adolescent and Young Adult (AYA), Acute Lymphoblastic Leukemia (ALL), Adverse Event (AE), Relative Value Unit (RVU), Children’s Oncology Group (COG), American Society of Hematology (ASH), Responsible Investigator (RI), Standard Operating Procedure (SOP), Primary Care Provider (PCP), Continuing Education (CE), Nurse Practitioner (NP), Advanced Practice Nurse (APN).
Figure 2.
Coding frequency of themes by focus group type and identification as either a barrier or facilitator for documentation and delivery of NCCN-concordant care for AYAs with ALL. Main themes (all caps) and sub-themes (denoted under corresponding main theme) were generated by all focus groups throughout study period. Facilitators are displayed in lighter shade and numbered closest to y-axis; barriers are in darker shade and numbered furthest from y-axis. All statements coded by sub-theme are also coded by corresponding main theme; however, not all statements coded by main theme are also coded for by sub-theme
3.2.1. Delivery of GCC
Five main themes with 15 associated sub-themes arose for delivery of GCC, with Supportive Care and Care Organization most frequent, followed by Individuals (Provider Factors and Patient Factors capturing specific behaviors or beliefs). Healthcare professionals across FG types identified Supportive Care (e.g., psychosocial factors) as the primary influence for AYA ALL care delivery, mostly as facilitators for AYA Services and Psychosocial Support. Care Organization ranked similarly, with strong sub-themes of Communication & Collaboration, External Partnerships & Collaborations, and Provider Education. Individuals ranked third, mostly due to Patient Factors like adherence presenting barriers to GCC delivery. The remaining two of the top five delivery themes included Care Model and Therapeutic Approach .
Prominent sub-themes within Supportive Care included Psychosocial Support and AYA Services. Presence of Psychosocial Support (reflected in top-ranked statements as assistance scheduling appointments and navigating care-related finances) was emphasized as a facilitator to initiating and completing GCC by non-physicians and physicians: “… reminding them of their therapy schedule, inpatient or outpatient, what to expect, what to bring, and timeframes” [Facilitator, Non-Physician, 2021]. Absence of this support is a noted barrier to GCC: “I don’t have all the [support] resources here that an AYA patient would need” [Barrier, Physician, 2021].
Across FG types, AYA Services facilitated GCC. Participants agreed in top-ranked statements that AYA-dedicated staff and resources, provider advocacy, and AYA-focused research improved care: “I think what would help would be, some type of [AYA] coordinator and navigator… it’s having a team approach. There’s a lot of different parts. And having everyone work together… helps when you all know you’re working towards something” [Facilitator, Mixed, 2019].
The Care Organization sub-theme External Partnerships & Collaborations was identified primarily as a facilitator across FG types, highlighting potential implementation strategies like sharing templated/standardized processes across institutions, embedded link/access to roadmaps within NCCN guidelines, open-sharing of roadmaps from COG protocols, and having AYA best practice care guideline(s) for all institutions: “There’s a lot of work…formulating those [Epic Beacon] plans and it would be wonderful if we’re all trying to standardize, including the NCCN guidelines to have that worked out and shared” [Facilitator, Mixed, 2019]. A leading barrier was complexity of AYA ALL care: “If you don’t have the clinical ability to see [AYA ALL]… then they’re never going to come to you in the first place” [Barrier, Physician, 2021].
Communication & Collaboration identified facilitation of GCC through multi-disciplinary teams, regularly scheduled team meetings, communication strategies, and pediatric/adult collaborations including sharing eligibility information to aid screening and cross-enrollment on trials: “For AYA who enter the adult institution first, the compliance with NCCN guidelines falls off pretty quickly… We now have folks embedded in the adult institution, so we’re able to monitor this more closely” [Barrier, Physician, 2021].
Provider Education identified lack of training in pediatric-inspired regimens as a barrier to GCC: “We didn’t get trained on pediatrically inspired regimens… [it would help to] learn… how they do things, and translate that into local community” [Barrier, Physician, 2021].
3.2.2. Documentation of GCC
Six main themes with 11 associated sub-themes arose for GCC documentation. Care Organization was overwhelmingly the most prominent theme across FG types, followed by Individuals and Supportive Care.
Within Care Organization , sub-themes of Electronic Medical Records (EMR) and Practice Standards & Expectations captured most coded statements. EMR emerged as a facilitator and barrier for documentation workflows. One participant suggested, “a checklist of what needs to be… documented [for GCC]” [Facilitator, Mixed, 2019]. Further, “sometimes the adult side is not aware of these guidelines as much as the pediatric side… it would be nice… if there is an AYA diagnosed, that the EMR is able to make what’s available as far as protocols for this population” [Facilitator, Non-Physician, 2021]. For Practice Standards & Expectations, notable barriers in top-ranked statements included lack of roadmaps (or not accessible), no documentation templates or consensus on documentation practices: “if someone’s not on study, particularly, I think the documentation gets a little more lax. And things that are part of the NCCN guidelines might not be included in your daily note” [Barrier, Physician FG, 2021].Suggested facilitators in ranked statements included strong research staff, use of “dot phrases,” and staff/provider training to standardize documentation.
For Individual Factors , all groups, but particularly physicians, described barriers around Provider Factors that impact documentation of GCC. In ranked statements, knowledge of AYA ALL NCCN guidelines and subjective treatment practices influence the likelihood of documenting GCC: “I will just confess I don’t look at the NCCN guidelines. I regard them as something to look at for something I’m not as familiar with treating. So, in sum, I think just an actual lack of familiarity or awareness of those particular guidelines for ALL” [Barrier, Physician FG, 2021].
Supportive Care was a leading theme for non-physician and mixed groups, noting potential to facilitate GCC documentation through enhanced patient assistance (e.g. designated navigators, oral medication calendars, and medication education).
4. Discussion
This study describes structure- and process-level barriers and facilitators impacting GCC among AYA with ALL, as identified through FG participation and use of nominal process. Themes of Care Organization , Supportive Care , and Individuals ranked highest for both delivery and documentation of GCC. Findings further identify targetable areas to increase GCC and improve AYA ALL outcomes.
Data support that optimization of care for AYA ALL has no one-size-fits-all solution, and heterogeneity across clinical facilities, ranging from aspects of the health systems and resource environments to multi-disciplinary teams, must be considered when tailoring practical implementation strategies for diverse patients, providers and systems. Identified barriers and facilitators to GCC can be linked to implementation strategies and incorporated into existing frameworks supported by prior NCORP-focused cancer care delivery research, 35 thus populating a blueprint of actionable next-steps (Figure 3). Example approaches include standardized trainings, bundled toolkits, population-specific checklists and algorithms, and practice protocols, though further work is needed to identify which strategies function best across practice settings, accounting for variation in facility structure/organization, patient population, and practice capacity.
Figure 3.
AYA ALL Cancer Care Delivery framework adapted to include NCORP-proposed Specific Multi-Level Implementation Strategies (adapted from Beauchemin M, et al, JAYAO, 2023). Implementation Strategies are derived from ranked statements, listed in full in Table 2
Discussion from these FGs were consistent with findings previously reported by our team, specifically the important role of model of care (adult-only, pediatric-only, mixed) at the CF where care is being delivered. 30 While many adult-only (60%) and pediatric-only (40%) CFs had an average annual AYA ALL volume of <5/yr, more adult CFs saw ≤10/yr (adult: 94%, pediatric: 73%, mixed: 62%). Nevertheless, in multivariable analysis only facility model was associated with delivery of guideline-concordant care (adult vs. ped+mixed: OR=0.02, 95%CI, 0.00-0.18) while AYA ALL volume was not associated with guideline-concordant care. 36 Pediatric and mixed CFs also reported more interaction between pediatric/adult oncology teams (tumor boards, initiating contact, or having an established counterpart) than adult-only practices. 30 It may follow then that limited interactions or collaboration opportunities between pediatric and adult oncology in adult-only settings further challenge pediatric-inspired treatment regimens which may be unfamiliar.
Many barriers and facilitators described during FGs directly support evidence-based strategies as process measures that can improve implementation of GCC, reducing AYA ALL outcome disparities. Since these specific strategies function within components of a healthcare delivery model, it is imperative to study them in a multi-level context. Adapting the published AYA cancer care disparities framework, 35 these strategies can be grouped by patient-, provider-, institution-, and system/policy-level (Figure 3).
Multi-level implementation strategies were identified using exploratory qualitative inquiry that leveraged the expertise of diverse healthcare professionals, providing evidence to support improvement in GCC as a sustainable intervention for AYA ALL. Across FG themes, specific patient-level strategies included local housing access for out-of-town AYA, personalized medication calendars and treatment reminders, health literacy information, and involvement from a caregiver. Concrete provider-directed strategies elicited in FGs included AYA-specific education, hands-on training, provider advocacy for AYA, recurring team meetings to improve communication, and opportunities for collaboration between adult and pediatric providers like COG members for medical oncologists. Institution-level implementation strategies included identification of AYA champions and psychosocial support staff, pharmacy engagement, pediatric and adult collaborations, AYA advocacy from cancer center leadership, and open-sharing of roadmaps and eligibility information to aid clinical trial cross-enrollment. Additional pragmatic tools included standardized order sets that bundle treatment, labs, and supportive care, along with institutional guidelines to dictate location of care for AYA with an established referral process. Specifically, physician FGs highlighted the “complexity of care for the patient population” when discussing these strategies in support for GCC for AYA ALL. Finally, notable strategies addressing system- or policy-level factors included prioritizing AYA-focused research and creating pathways for sharing standardized/templated processes for AYA cancer care across institutions, including a national AYA best practice care guideline. Opportunities to improve NCCN guidelines themselves were suggested, like providing roadmaps and other materials for recommended regimens to enhance accessibility and navigation. As guideline content continues to evolve (2025 NCCN ALL guidelines specify pediatric-inspired therapy for AYAs without significant comorbidities 37 ; 2026 NCCN AYA guidelines reference ALL guidelines for therapy). Of note, the American Society of Hematology recently issued guidelines regarding frontline therapy for AYAs with ALL, with a recommendation for pediatric-inspired therapy along with supportive care recommendations. 38 Whether these address some of the FG suggestions warrants further examination.
The potential application of these findings reaches far beyond the NCORP. Capacity for AYA cancer care varies greatly across community-based practices. Recent assessments of diverse practice settings can improve generalizability of findings, providing further insight regarding resource limitations that may impact both AYA access to cancer care and the feasibility of strategies to improve GCC. Among 271 practices participating in the 2022 NCORP Landscape Assessment, 37% met one of the AYA cancer care capacity criteria (self-identify as having an AYA Program, treat ≥50 AYAs with cancer/year, and/or AYA comprising ≥5% of annual cases), of which only 20% reported having AYA-specific resources. 39 Among the 84 practices participating in ACCL16N1CD that saw ≥1 AYA with ALL/year, most (79%) had no AYA-specific resources. 30 However, AYA capacity remains limited outside community settings also; even among NCI-designated Comprehensive Cancer Centers, only half report having AYA oncology programs. 40 Future AYA care delivery studies across NCORP and non-NCORP practices should incorporate an inclusive up-front approach with scalable implementation and dissemination strategies.
These findings must be considered in the context of study limitations. FG data represent a fraction of healthcare professionals caring for AYA ALL; however, diverse sampling across NCORP characteristics and roles sought to optimize representative participation of practice settings. Also, two different participants joined in two FGs that were two years apart, though any redundancy was likely offset by NGT procedures and achieving saturation of ideas across FG types. The timing of FGs began prior to the COVID-19 pandemic (2019) and continued through peak pandemic years (2023) which may have placed unknown stressors on practice settings and healthcare professionals impacting volunteerism; on the other hand, shifting from an in-person to virtual format may have enhanced accessibility for professionals from some practices. In addition, while healthcare professionals across participating NCORP practices were invited to participate, the distribution of FG volunteers (adult: 17%, pediatric: 43%, mixed: 41%) may limit the contribution of unique experiences faced in adult-only settings related to pediatric-inspired therapy. That being said, the voice from mixed CFs is important to include in that while more participating CFs were adult (adult: 55%, pediatric: 17%, mixed: 28%), with substantial variation in annual volume of AYAs with ALL (very low at most models), more AYAs were treated at mixed CFs (adult: 30.4%, pediatric: 29.5%, mixed: 40.1%).
5. Conclusion
This study identified barriers and facilitators related to themes of Supportive Care and Care Organization that can impact the proportion of AYA with ALL receiving treatment according to NCCN guidelines. Implementation strategies derived from FGs of healthcare professionals caring for AYA ALL at NCORPs provide guidance for future care delivery studies with the potential to inform institutional and national changes to practice and policy. Ultimately, these findings inform an intervention roadmap with actionable steps for implementation toward providing equitable, high-quality, evidence-based care to all AYA with ALL.
Supplemental Material
Supplemental Material for Adolescents and Young Adults With Acute Lymphoblastic Leukemia: Qualitative Barriers and Facilitators to Guideline-Concordant Care by Allison C. Grimes, MD, MSCI, Julie A. Wolfson, MD, MSHS, Charlotte L. Kerber, MS, Kristin M. Bingen, PhD, Melissa P. Beauchemin, PhD, RN, CPNP-PC, CPON, Koh B. Boayue, MD, Jennifer M. Levine, MD, MSW, Michele A. Scialla, MSN, RN, CCRC, Wendy L. Woods, MD, MPH, Jane J. Liu, MD, Olivia Ponce, BA, Sarah L. Vargas, PhD, Anjali S. Advani, MD, George J. Chang, MD, MS, MHCM, Emily K. Curran, MD, Dawn L. Hershman, MD, MS, FASCO, Selina M. Luger, MD, Kristen M. O’Dwyer, MD, Wendy Stock, MD, David S. Dickens, MD, Michael E. Roth, MD, David R. Freyer, DO, MS, Brad H. Pollock, PhD, MPH, Lillian Sung, MD, PhD, Susan K. Parsons, MD, MRP in Cancer Control.
Acknowledgments
The authors would like to acknowledge the efforts of all the participating NCORP sites and staff, whose work contributed significantly to the project presented above. The authors are especially grateful to Tammy Lo for her contributions to the conduct of this analysis. This work would not have been possible without the collaboration of the following groups from the noted NCORP Research Bases, as represented by the identified co-authors: Alliance Cancer Care Delivery Research (G.Chang) and Leukemia (W.Stock, E.Curran) Committees along with the Alliance Community Oncology Co-PI (J.Liu), SWOG Cancer Care Delivery (D.Hershman) and Leukemia (A.Advani, K.O’Dwyer) Committees, and ECOG-ACRIN Leukemia Committee (S.Luger). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Funding: The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was funded by the Children’s Oncology Group (COG) NCI Community Oncology Research Program (NCORP) Research Base grant [UG1CA189955, MPI: Roth, Pollock] and COG grants U10CA180899 [PI: Alonzo] and U10CA180886 [PI: Hawkins], along with NCORP Research Base grants for the Alliance for Clinical Trials in Oncology [UG1CA189823, MPI: Paskett, Galanis, Hahn], SWOG [UG1CA189974, MPI: Blanke, Hershman, Tangen], and ECOG-ACRIN [UG1CA189828, MPI: Wagner, Schnall]. LS is supported by the Canada Research Chair in Pediatric Oncology Supportive Care.
The authors declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: All Authors listed have seen and approved the manuscript being submitted, the article is the Authors’ original work, the article or research has not been submitted for publication nor has it been published in whole or in part elsewhere (excepting abstracts published as part of meeting materials), all Authors are prepared to assign copyright to Cancer Control upon acceptance of the manuscript, the corresponding Author shall bear full responsibility for the submission on behalf of all Co-Authors, and all Authors listed on the title page have contributed significantly to the work.
Disclaimers: This study has not been previously presented or published publicly.
Supplemental Material: Supplemental material for this article is available online.
ORCID iDs
Allison C. Grimes https://orcid.org/0000-0001-5729-2778
Michele A. Scialla https://orcid.org/0000-0001-7933-0675
Wendy L. Woods https://orcid.org/0000-0002-6280-5360
Ethical Considerations
The study was approved by the NCI Pediatric Central Institutional Review Board (IRB) on September 1, 2017. Documentation of consent requirement was waived by the IRB given the nature of the study.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Supplemental Material for Adolescents and Young Adults With Acute Lymphoblastic Leukemia: Qualitative Barriers and Facilitators to Guideline-Concordant Care by Allison C. Grimes, MD, MSCI, Julie A. Wolfson, MD, MSHS, Charlotte L. Kerber, MS, Kristin M. Bingen, PhD, Melissa P. Beauchemin, PhD, RN, CPNP-PC, CPON, Koh B. Boayue, MD, Jennifer M. Levine, MD, MSW, Michele A. Scialla, MSN, RN, CCRC, Wendy L. Woods, MD, MPH, Jane J. Liu, MD, Olivia Ponce, BA, Sarah L. Vargas, PhD, Anjali S. Advani, MD, George J. Chang, MD, MS, MHCM, Emily K. Curran, MD, Dawn L. Hershman, MD, MS, FASCO, Selina M. Luger, MD, Kristen M. O’Dwyer, MD, Wendy Stock, MD, David S. Dickens, MD, Michael E. Roth, MD, David R. Freyer, DO, MS, Brad H. Pollock, PhD, MPH, Lillian Sung, MD, PhD, Susan K. Parsons, MD, MRP in Cancer Control.