Oncologists' Perspectives on Oncology Stewardship: A Focus Group Exploration in a Statewide Quality Improvement Consortium.

Introduction

Establishing the Need for Oncology Stewardship

The treatment landscape in oncology is ever-expanding and increasingly complex. In 2023, the Food and Drug Administration (FDA) approved 26 novel cancer therapies. 1 Of these, over 50% were based on single-arm studies with a primary endpoint of overall response rate. Of 12 therapies with comparative studies lending basis for approval, only three showed improvements in survival. 2–4 Five bispecific antibody therapies were approved yet none of the approvals were based on comparative trials despite four of the bispecifics being targeted at the same two diseases (two for multiple myeloma and two for diffuse large B-cell lymphoma) with nearly identical indications. 5–8 While actively evolving at the time of this writing, only some of these agents have had a comparator trial completed. In those trials, it was the combination of bispecific therapies and traditional agents, that showed improvements in efficacy over comparators. Additionally, in some cases while listed as options in national guidelines, the comparators would arguably not be the best standard of care for the populations studied. 9–12 In 2024, this trend continued with 18 novel approvals, of which only eight were based on a comparative trial, and none of which showed survival improvements at the time of approval. 1 The number of approvals based on low-quality evidence creates uncertainty regarding the best treatment approach for individual diseases and escalates the cost of care without commensurate improvements in survival outcomes in the United States. 13 , 14

Various models have sought to emphasize value-based care or contain costs associated with cancer care. Payers have attempted to control costs through multiple avenues including prior authorization requirements, product preference selection of biosimilars or generic agents, or site-of-care initiatives. Health systems have used formulary restrictions or clinical pathways. Oncology organizations have incorporated value into clinical decision-making and education. These tools are, however, limited in the scope of cost analysis (drug cost only, not incorporating global costs of therapies) and may not use value assessments to differentiate among multiple treatment options. 15 Patient outcome reporting from these various models is variable with positive impact seen in some settings where pathways have been implemented and unknown impact of payer and formulary restrictions. Oncology stewardship refers to a set of coordinated strategies to improve the use of systemic anticancer therapy with the goal of enhancing patient health outcomes while reducing financial toxicity. 16–18 It is a comprehensive approach to care that focuses on using evidence-based medicine to improve patient outcomes, enhance quality of life, and optimize resource utilization. By promoting evidence-based practices and interprofessional collaboration, stewardship reduces variation in care and minimizes toxicity, including financial toxicity. 19 As with antibiotic stewardship programs, oncology stewardship can help providers optimize resource use and reduce costs while emphasizing clinician-driven decision-making, which is an important distinction from other options, such as clinical pathway programs. Principles of stewardship have been applied in some limited settings, including appropriately allocating cancer-directed therapy during drug shortages, reducing inpatient drug expenditure, and reviewing novel agents in the treatment of various hematologic malignancies. 16 , 20–23 Currently, however, there are no models for creating an oncology stewardship program that can be applied across oncology practices that differ in institutional size and resources, variety of cancer types treated, and patient populations served.

Exploring a Conceptual Framework for a Statewide Stewardship Program

The Michigan Oncology Quality Consortium (MOQC) is a collaborative of hematologist-oncologists and gynecologic oncologists in Michigan, representing nearly all practices in the state. 24 MOQC’s purpose is to further the success of interdisciplinary teams that improve the quality and value of cancer care across the state. MOQC has accomplished this through quality improvement initiatives across a variety of aspects of the cancer journey. 25–27 Oncology stewardship was introduced to MOQC practices during the winter consortium biannual meeting held in January 2023. After establishing interest in the concept of stewardship from members and obtaining support from the MOQC Patient and Caregiver Oncology Quality Council (POQC), MOQC sought to explore strategies to implement a statewide stewardship program.

The authors first refined the definition of oncology stewardship using the framework put forth by The Society of Healthcare Epidemiology of America (SHEA) in infectious diseases, including guidance from work defining value in healthcare and oncology outlined by the Institute of Medicine. 28–31 Next, the goals and tenets of stewardship were developed using a backbone of evidence-based medicine (EBM), which translates evidence into practice by integrating clinical expertise and stakeholder values in decision-making. 32 Engaging patients in decision-making and improving access to care were both incorporated into the tenets via encouragement of rational use of services, open discussion about financial toxicity, and promotion of interventions that improve quality of life. These goals and tenets were presented at the winter MOQC biannual meeting. To assess feasibility of a statewide stewardship program, we examined perceptions of a sample of MOQC physicians.

This report describes the formation and results of our focus groups eliciting thoughts and perceptions about oncology stewardship and challenges in implementing a statewide program.

Methods

We conducted two professionally led focus groups in preparation for the creation of a statewide oncology stewardship proposal and implementation plan.

Rationale for Format

The purpose of this project was to gather insight from physicians in various clinical settings and sub-specialties within hematology/oncology to provide direction to the initiative. We sought to better understand needs in clinical evidence interpretation, how a stewardship initiative could meet those needs, and potential barriers to implementing a program. To facilitate these goals, a focus group discussion format was selected.

Participant Selection and Recruitment

At regional MOQC meetings in spring 2023, physician champions for all 71 MOQC practice sites were asked to nominate one hematologist and one oncologist whom they considered to be thought leaders across the state of Michigan. Thought leaders were defined as people whom the respondent would contact in the case of a clinical question or dilemma. Physician champions could nominate themselves.

All nominated physicians were invited via Email to participate in one of two two-hour focus groups with the goal of eliciting thoughts and ideas about oncology stewardship (as defined as above in the invitation). Focus group participants were informed that, although the focus groups would be recorded, no identifying information would be shared in written reports or any other form. All participants consented to participation and dissemination of findings including publication of anonymized responses. Participants were asked to disclose any relationships with industry for themselves and their family members. Participants were provided with an honorarium of $400 ($200/hour).

Project Lead Characteristics and Reflexivity

The project team was composed of oncology board-certified pharmacists with clinical practice experience in malignant hematology and oncology and stewardship expertise, a physician with medical oncology, health services, and public health expertise, and a qualitative research expert who facilitated the focus groups discussions.

A discussion guide was created by the pharmacists (LLB, AJS, ESM), in consultation with qualitative researcher (KG) and the oncologist (JJG) (available in Supplementary Appendix ). The project leads (LLB, AJS, ESM, JJG) met weekly throughout summer and fall of 2023 to discuss preconceptions, biases, and reflections. The qualitative research expert, who was naïve to the concept of oncology stewardship before project involvement, served as the focus group facilitator. The neutrality and naivety of the facilitator was intentional to reduce bias or leading the participants in any way. Additionally, the project leads debated whether the focus groups participants should include pharmacists given that stewardship principles are often emphasized in pharmacists’ training and because they are integral members of stewardship efforts across a variety of disease states. 29 , 33–36 Because the goal for this segment of the project was to solicit the opinions of prescribers, and because their training and perspective around stewardship principles may differ from pharmacists, the decision was made not to include pharmacists in the focus groups.

Data Collection

Focus groups were led virtually on Zoom (September 27 and November 6, 2023) by the same trained facilitators from the University of Michigan Institute for Social Research. Focus groups lasted two hours with a scheduled brief break. Participants watched a 3-minute video introducing oncology stewardship created by the study team. 37 The discussions were recorded for later transcription. Illustrations of topics discussed in each session were created by a professional visual recorder to capture the main themes and the ways in which they relate to one another.

Open-ended questions were posed to address the following topics: 1) impressions of oncology stewardship: the discussion elicited reactions from the video presentation on principles of stewardship, goals of a stewardship initiative, benefits of stewardship to clinical practice, concerns about implementing stewardship, and goals and tenets of the initiative, 2) new approvals through the stewardship lens - two hypothetical clinical scenario-based questions were presented to understand how providers currently practice stewardship, and 3) ways in which to operationalize a stewardship program and perceived barriers to stewardship programs. Full details on each component are included in the discussion guide which is available in the supplementary Appendix .

This project was deemed exempt from human subject review by the University of Michigan Institutional Review Board (HUM00241036).

Data Analysis

Choice of Approach for Qualitative Analysis

A summary report was generated by the facilitators, who did not have a clinical background and had expertise in qualitative analysis, after both focus groups had been completed. The report was drawn from thematic analysis of the participants’ comments in the group discussion. This is a qualitative descriptive approach that identifies patterns or themes in the group commentary and summarizes this data to guide decision-making and inform processes or procedures to meet the needs of the population under study. The author group reviewed and discussed the summary. Given the relatively small sample size, no formal coding scheme or software was used. To add credibility to the findings, member checking was conducted by sharing preliminary themes with the participants, whose feedback was used to confirm, refine, and clarify the thematic interpretation.

Sample Size Justification

We sought to include clinicians from both large academic medical centers and smaller community-based practices, representing a broad range of sub-specialties. We achieved this across both groups, with at least one physician participating from each of these specialties: hematology, gynecologic oncology, and multiple solid tumor disciplines. To understand and meet the needs of practices in the geographically and demographically diverse areas of Michigan, MOQC divides the state into six regions (defined at https://moqc.org/moqc/members/ ). The region of all participants was recorded.

Endpoint

The thematic summary was reviewed by the research team. A third member checking session was held between the focus group participants and project leads (February 13, 2024) to ensure that the findings were adequately presented and the material summarized was representative of the collective group.

Results

Participant Characteristics

Nominations were received for 40 physicians, 22 in oncology and 18 in hematology, who were then invited to participate. Of these, 9 oncologists and 5 hematologists expressed interest. The 2 sessions were attended by 13 participants, 8 in the first and 5 in the second. Five of the 6 MOQC regions were represented ( Supplementary Figure 1 ). Four participants were members of small practices (1 to 5 physicians), 1 was from a medium practice (6 to 14 physicians), and 8 were from large practices (15 or more physicians). Hematologists (n = 3) and oncologists (n = 9) participated in addition to one physician who sees both hematology and oncology patients ( Supplementary Table 1 ). Focus group participant relationships with industry are included in the Supplementary Appendix .

Impressions of Oncology Stewardship

Participants primarily associated stewardship with patient advocacy and quality care delivery, and secondarily with cost effectiveness or judicious use of resources. Stewardship was described as helping to balance the dual need to advocate for individual patients and to consider societal costs and benefits. Overall impressions on stewardship from the discussion captured as an illustration by a visual recorder are presented in Figures 1A and B .

Benefits to and Concerns About the Implementation of a Stewardship Initiative

Participants expressed the belief that stewardship could benefit their clinical practices and address challenges they face in several ways, including promoting advocacy for patients through raising awareness of costs. Participants believed that increasing awareness of costs could encourage pharmaceutical companies to improve access and could increase pressure on manufacturers to lower costs. Cost transparency, perhaps through embedding costs within national guidelines, could make prescribers more cost-conscious and encourage pharmaceutical companies to reduce prices.

Participants speculated that, using the principles of stewardship, prescribers could apply a value-based approach to understand the real benefits of treatment interventions. While clinical decision-making is presumed to be left to the prescriber judgment, EBM aids that include quantitative metrics such as a comorbidity index or analysis of life expectancy and impact on quality of life could provide more concrete data to guide the treatment pathway. This could assist oncologists in making choices based on both the strength of evidence and the relative value of treatments. Finally, guidance on sequencing treatment options is a critical need and determining when referrals to clinical trials might be appropriate.

Goals and Tenets of Oncology Stewardship

The three goals of a stewardship initiative were presented to the participants ( Table 1 ). Participants endorsed these goals and were particularly interested in the last two: evidence-based, clinician-driven decision-making and collaborative evaluations of new approvals.

The five tenets of stewardship practice were presented ( Table 1 ). Participants broadly endorsed the goals and tenets of stewardship, and many expressed already employing many of these tenets in their practices. However, participants described their experience with financial information often being opaque and reported difficulty estimating out-of-pocket cost to patients. When evaluating new therapies, efficacy and safety information is available, but the cost of new therapies on both a societal and individual patient level is generally not. Furthermore, financial information is difficult to incorporate into conversations with patients.

Evaluating New Approvals Through a Stewardship Lens

When asked about the most important aspect of evaluating the results of a clinical trial, eight participants selected “comparator arm that is consistent with best standard of care”, three selected “primary endpoint of the study is overall survival”, one chose “primary endpoint is a surrogate such as progression free survival, overall response rate, or complete response”, and no participants chose “presence of a comparator arm” ( Figure 2 ). They endorsed the clinical context as well as the availability of other treatment options as meaningful considerations in a prescribing decision involving therapies that had shown benefit to an inferior comparator. They would be inclined to prescribe such a drug if there was a lack of better alternatives or if the drug presented advantages in terms of cost, toxicity, and accessibility.

When asked about reasons for prescribing therapies with insufficient evidence of benefit, six participants chose “therapies are endorsed by guidelines”, and five chose “therapies are approved by the FDA.” One participant chose “other”, and no participants selected “because a patient/caregiver is requesting” or “because colleagues inside or outside of Michigan are prescribing” ( Figure 2 ). Regarding guidelines that influence prescribing options, participants identified National Comprehensive Cancer Network (NCCN) as the most influential. Participants expressed skepticism towards FDA approvals noting that approval was not always sufficient for integration into clinical practice. Representative quotes are shown in Table 2 .

Clinical Scenarios

Scenario 1 - Drug A is compared against a non-standard of care therapy and it shows overall survival benefit. You disagree with the way the study was performed and its conclusions, but the drug is added to national guidelines as a Category 1 recommendation. How likely are you to prescribe this drug?

Participants agreed that the clinical context and the availability of other treatment options would be significant considerations in a prescribing decision involving this medication. They would be inclined to prescribe Drug A if there were a lack of better alternatives or if Drug A presented advantages in terms of cost, toxicity, and accessibility. In considering Drug A, physicians would be transparent with patients; several indicated they would discuss Drug A as a potential choice with them but would include their concerns about the way the study was conducted.

A few participants expressed hesitation about prescribing Drug A if they had reservations about the study methods or conclusions. They were, however, more likely to weigh their clinical experience and the “real-world” experience when they faced limited options in available treatments. In addition, they pointed out that time between when the study leading to approval was conducted and when the approval was granted can play a role in decision-making, particularly in cases where other alternative treatments also become available.

While critical of sub-standard or lack of control arms in clinical trials, physicians would still use therapies such as Drug A if they felt it was the best available for their patients. This is particularly true for orphan diseases where there are limited treatment options. Participants expressed greater confidence in treatments whose approval trials align with their perceptions of best practice but could readily present situations that would be exceptions.

Scenario 2 - Drug B is approved based on a single-arm study with primary endpoint of overall response rate (accelerated approval) while a comparative trial is ongoing, and the drug is added to national guidelines. How likely are you to prescribe this drug?

Physicians identified situations where single-arm studies may be appropriate. They indicated a greater interest in considering these options in situations where treatment options are limited while acknowledging that they are making the choice with less than optimal (or preliminary) trial results.

Several examples were shared, including medications that were withdrawn after an initially promising trial, such as belantamab mafodotin, and those that were more successful, including several targeted agents (crizotinib for ALK-positive lung cancer, entrectinib for tumors with NTRK fusions). There was general agreement that, conditional on the toxicity and the efficacy demonstrated in the single-arm study, Drug B would be considered despite the drawbacks of the trial.

Representative Quotes Relating to Scenarios 1 and 2 Can Be Found in Table 2

How to Operationalize a Statewide Oncology Stewardship Vision

Participants were asked to choose which implementation strategy would be most positively impactful to their practice. Of the five choices provided, eight of twelve participants selected “resources provided by MOQC for providers that appraise data for new approvals in a standardized fashion and in context of other available therapy options” as the most impactful. Three selected “clinical disease state pathways developed by clinicians across the state” and one selected “devoting a portion of biannual MOQC meetings to discussion of new approvals and consensus building around guidelines for use” ( Figure 3 ). No participants selected “patient-facing resources that educate patients on new therapies” or “formulary that is agreed on by all MOQC sites.”

There was agreement that a resource to assist in evaluating data for new approvals in a standardized fashion would be beneficial. Participants acknowledged that several entities (eg, NCCN and American Society of Cancer Oncology (ASCO)) that have developed tools for evaluating value, but there is lack of clarity as to the frequency of updates to these and how/if newer therapies result in updates to the evaluations for other therapies. 32 , 33 Finally, participants shared that they had a limited understanding of these tools. They believe that most clinicians find the methodology difficult to understand and struggle with interpreting them, which limits their applicability in everyday practice.

Discussion

In this focus group study of oncologists in Michigan, participants expressed interest in statewide oncology stewardship initiatives and endorsed the tenets presented. The predefined MOQC stewardship program goals of “evidence-based, clinician-driven decision-making and collaborative evaluations of new approvals” resonated most with the providers. Oncology stewardship has the potential to clarify the value of therapies at individual and societal levels and guide sequencing options, both which can reduce variability in care. 28

Evaluating drug approvals through the lens of stewardship, however, revealed dissonance between the importance participants assigned to rigorous trial design and their prescribing behaviors. Specifically, participants justified the acceptance of lower quality evidence in clinical scenarios presented even when disagreeing with study methodology despite an overall high importance placed in having clinical trials that utilized appropriate comparator arms. Reasons for this dissonance included heavily placed trust in consensus guidelines, a lack of other treatment options, and, in specific cases, a favorable evaluation of the therapy’s toxicity, cost, and access compared to alternatives. This reflects the complex, high-stakes decision-making and challenges presented by ever-expanding arsenal of treatments, and, at times, unclear benefit of the individual therapies in that arsenal. This tension represents an important finding with direct implications to the ability to implement stewardship in this space. Oncology stewardship efforts must address not only evidence appraisal, but also clinical urgency, guideline influence, limited alternatives, and patient-centered pressures that shape real-world prescribing. Similar tensions between intention and behavior have been documented in antimicrobial prescribing, and recent literature highlights the prevalence of this as a barrier to successful implementation of stewardship efforts as well as the importance of constant updated streamlined education to help mitigate these barriers. 38–40

The costs of cancer care are rising faster than in any other disease, and frequent new approvals overwhelm providers, especially those treating multiple malignancies. Despite higher spending, United States cancer outcomes have not improved compared to other countries. 15 While ongoing efforts to promote trial designs that prioritize meaningful outcomes, there is an urgent need to provide resources that allow providers to evaluate therapies approved in the absence of robust evidence of meaningful benefit. 41

Tremendous non-clinical variation exists in the care given to patients according to practice, individual clinician, or patient place of residence perpetuating outcome gaps based on the resources access. When therapies are approved without strong evidence of benefit over standard of care, their real-world benefit may be limited. 42 , 43 Some examples of these types of therapies include bispecific antibodies and chimeric T-cell therapy, many of which have been approved under accelerated programs. 5–8 The incorporation of these treatments is extremely resource-intensive and inherently discriminatory in who can benefit from them both in the clinical trial phase and after approval. 44 , 45 Including these therapies as standards of care in national consensus-driven guidelines may encourage the perception that these therapies should be prescribed regardless of the frailty of the evidence that supports their approval and without a robust understanding of their optimal place in therapy. 46 Consensus-based guidelines in the United States may recommend therapies that have little or no improvement in disease outcomes but are considered “desirable” without a definition of what desirable means. MOQC oncology stewardship aims to reduce care variation by providing resources that help clinicians make informed decisions relating to the value of therapies. Individual oncology practices in Michigan have variable access to resources like peer oncologists, disease state experts, the ability to create institutional guidelines, financial access tools, and clinical pharmacist support. Such resources would allow for dissemination of information regardless of practice resources and patient case mix.

Our participants were highly interested in resources provided by our collaborative to evaluate the value of novel therapies. This suggests that providing context about how novel approvals compare to other options in the current treatment landscape may fill a need not currently met by guidelines. Participants placed special emphasis on clinician-driven decision-making when creating statewide resources. This is an important distinction from other available options, such as clinical pathway programs. While studies have shown pathways to be successful in reducing variability in care and decrease costs while maintaining efficacy in some scenarios, these products may constrain individualized care. 47 , 48 Prescribing restrictions are not appealing given existing mechanisms that restrict care such as prior authorizations. Other possible implementation strategies, such as a statewide formulary, are likely infeasible due to diverse physician organizations and conflicts with health systems’ formularies.

These focus groups brought together a group of oncologists and hematologists representing most regions in the state and all practice sizes. The clinical experiences of prescribers shaped a potential statewide stewardship initiative. While discussions centered on appraisal of new drug approvals, the concepts of developing a shared goal and gaining consensus from a diverse group of practitioners are applicable to other resource utilization challenges.

Our work has some notable limitations. While members of various disciplines and settings within hematology/oncology were represented, the total number of participants was small. Additionally, there may be some response bias introduced based on the nomination process, and it is possible that providers who chose to participate may have done so because of interest in stewardship. The smaller number of participants allowed for rich conversation and ability of the facilitator to elicit responses from all and maintain engagement of the group throughout the entire session. Nonetheless, the findings reported are merely suggestive of the positive perception of prescribers towards stewardship. Additionally, while cognitive dissonance was noted with hypothetical scenarios discussed, this is merely suggestive of what would occur in actual practice, and confirmation of this dissonance in practice would need further confirmation. Further dissemination of findings will elicit input from all MOQC members to explore future directions.

Given ongoing interest, a series of pilot disease specific implementation projects were presented. This effort will validate the findings of this focus group exploration among the interdisciplinary teams that are involved in care across the state, and will determine feasibility and scalability, address implementation barriers, and identify resource requirements. We will engage with non-physician practice members including pharmacists, administration personnel, and POQC in the development of this effort. Based on feedback gathered and findings of our pilot implementation project, the creation of a statewide oncology stewardship program will move forward in MOQC. Future work will be done to identify therapies, diseases, and indications for therapies that may be eligible for a stewardship approach.

Conclusion

In this statewide quality improvement collaborative, focus group participants supported stewardship principles and oncology stewardship program goals. They acknowledged high levels of trust in national guidelines for complex clinical decision-making, even when supporting evidence is weak, which may at times present a challenge to stewardship implementation. They saw value in MOQC resources to promote evidence-based, collaborative practice and reduce care variation, and these resources should address real-world pressures that influence treatment decisions. A stewardship program may support consistent high-quality care while maintaining therapy access.

Acknowledgments

Lydia L Benitez and Allison J Schepers are co-first authors for this study. Although Blue Cross Blue Shield of Michigan (BCBSM) and Michigan Oncology Quality Consortium work collaboratively, the opinions, beliefs and viewpoints expressed by the authors do not necessarily reflect the opinions, beliefs, and viewpoints of BCBSM or any of its employees.

Funding Statement

Support for Michigan Oncology Quality Consortium is provided by Blue Cross and Blue Shield of Michigan as part of the BCBSM Value Partnerships program.

Disclosure

Dr Lydia Benitez is the Chair of Practice Outcomes and Professional Benchmarking Committee (POPBC) – volunteer role for Hematology Oncology Pharmacists Association. Dr Allison Schepers reports honoraria from PTCE and leadership or fiduciary roles as the chairperson of BCOP Annual Conference Committee for HOPA, outside the submitted work. The authors report no other conflicts of interest in this work.

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