Studying the Implementation of Exercise Oncology Interventions: A Path Forward : Translational Journal of the American College of Sports Medicine

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Implementation Science

Studying the Implementation of Exercise Oncology Interventions: A Path Forward

Adsul, Prajakta1; Schmitz, Kathryn2; Basen-Engquist, Karen M.3; Rogers, Laura Q.4

Author Information
Translational Journal of the ACSM: Fall 2022 - Volume 7 - Issue 4 - p 1-8
doi: 10.1249/TJX.0000000000000208

Abstract

INTRODUCTION

The number of cancer survivors living in the United States is 17 million and rising (1). Exercise is an effective strategy for managing negative sequela, improving quality of life, and reducing risk of cancer mortality and all-cause mortality in cancer survivors, yet most cancer survivors do not engage in regular recommended exercise (2–5). Therefore, a greater focus on the dissemination and implementation of exercise oncology evidence-based interventions (EBIs) is critical (2,6). Implementing an EBI in a real-world setting requires the consideration of not only the intervention itself but also the setting in which the intervention is delivered (e.g., clinical, community, administrative infrastructure, economic models) and the process of intervention delivery (i.e., who delivers the intervention and how, including interventionist training for ensuring the safety of supervised, structured evidence-based exercise oncology programs). Further, cancer survivors need information and motivation to engage with the intervention. For population impact, these critical components (see Fig. 1) require research to move beyond testing interventions for efficacy and toward a focus on the implementation of interventions in real-world settings. However, very few studies report on the implementation of exercise oncology EBIs in real-world settings, and data on strategies that increase success (i.e., implementation strategies) are almost nonexistent (7,8).

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Figure 1:
Real-world delivery of EBIs to help cancer survivors requires the consideration of the appropriate intervention, setting, and delivery while focusing on the cancer survivor needs and engagement.

Given the dearth of implementation-focused, peer-reviewed literature, the science of implementation relies extensively on theories, models, and frameworks that have been curated in a publicly available repository (9). Collectively, these contribute to building an evidence base for improving implementation efforts for EBIs. Some recent studies have specifically looked at exercise oncology–related implementation outcomes and evaluations of practice-based evidence (10,11). For example, a recent description of exercise program translation in Canada (one of the three programs targeted cancer survivors) used Knowledge to Action (a process model) and RE-AIM (Reach, Effectiveness, Adoption, Implementation, and Maintenance; an evaluation framework) (12). Other studies include that of Glowacki et al. (13), who used a classic theory (i.e., Diffusion of Innovations) to help explain the process of health care provider implementation of an exercise toolkit for patients with depression (not cancer survivors specifically). The widely used Exploration, Preparation, Implementation, and Sustainment (EPIS) framework is a comprehensive framework focusing on factors influencing implementation during different phases and at multiple socioecological levels (e.g., individual, organizational, and system) (14). It has informed implementation across a wide variety of intervention types and settings (15). What is unique about this framework is that it covers the core components of implementation while providing an overarching understanding of the process, determinants, and evaluation, thereby reducing the need for using multiple frameworks (16).

The limited knowledge around implementation barriers or potential implementation strategies that address these barriers in terms of exercise oncology prompted this study. The overall purpose was to identify common and differentiating aspects of the implementation process and strategies used in three different implementation efforts focused on exercise EBIs. We highlight a path forward for implementation science and exercise oncology EBIs while also providing practice-based evidence for future research efforts in implementing exercise oncology EBIs in real-world, clinical practice.

METHODS

The EPIS framework was well suited for this research because of its comprehensiveness and versatility with regard to intervention type and context. We used it to organize the three efforts focused on implementing exercise oncology EBIs in real-world settings by illustrating the pragmatic observations during one or more of the EPIS phases. The methods used in the individually described implementation efforts were primarily qualitative and, in some cases, observational. Three authors (K.S., K.M.B.-E., and L.Q.R.), with the help of the first author (P.A.), operationalized the strategies as they were used in their respective studies. To guide this process, we used the compilation of 73 strategies put forth by the Expert Recommendations for Implementing Change (ERIC) to define and operationalize the strategies used in the three efforts (17). Using the existing taxonomy (specifically Appendix 6 in Powell et al. (17)) allowed us to further strengthen our operationalization of the strategies and establish alignment with the current literature base in implementation science.

We also considered the nine overarching categories that map out the 73 discrete strategies in the second phase of the ERIC study (18). We used a systematic approach to compiling strategies, using a retrospective examination of the three implementation efforts across several years that are presented in this article. Such a methodology aligns with the calls in the field to improve tracking and reporting of implementation strategies for advancing the science of implementation (19). The information presented in this article could serve as a starting point for investigators promoting the implementation of exercise oncology EBIs. All four authors met several times to resolve differences and generate consensus to operationalize each strategy from the three different implementation efforts. Finally, all co-authors mapped the specific strategies onto the different EPIS phases, as used in their projects (shown in Fig. 2).

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Figure 2:
Compendium of implementation strategies used in exercise oncology implementation examples, arranged according to EPIS phases.

RESULTS

Project 1: Better Exercise Adherence after Treatment for Cancer (Principal Investigator: L.Q.R.)

EBI

Better Exercise Adherence after Treatment for Cancer (BEAT Cancer) is a 3-month, social cognitive theory–based exercise intervention proven efficacious by a multicenter randomized trial (20,21). The intervention includes 6 discussion group sessions (on topics such as time management, behavioral modification strategies, etc.) and 12 exercise sessions in the first 6 wk that are tapered to unsupervised, home-based exercise with biweekly exercise counseling in the last 6 wk (20). The intervention goal is to gradually increase aerobic physical activity to at least 150 weekly minutes of moderate-to-vigorous activity (20).

Implementation setting and intended population

We planned for implementing BEAT Cancer at a rural, community-level cancer care setting by adapting for women with any cancer type and developing an implementation toolkit. We identified a champion from our urban academic institution who facilitated rural implementation site selection, community partner approval, and grant proposal and start-up activities. Because our focus was on reaching rural populations, we identified a small community-based cancer care setting that was located in and served counties with Rural–Urban Continuum Code (RUCC) classification of completely rural, or <2500 urban population, adjacent (RUCC = 8) or not adjacent (RUCC = 9) to a metro area (22). Our target population included women who were rural residents with a history of any cancer type and physician clearance for participation (23). The implementation project was approved by the Institutional Review Board of the University of Alabama at Birmingham (protocol no. X150325007) and our community partner, Russell Medical Center (protocol no. 20160006). Informed consent was obtained before obtaining the resultant data.

Key implementation questions

This implementation effort focused on anticipated implementation barriers and facilitators in a rural, community-based setting. Combining this information with experience during efficacy testing in more urban locations supported our long-term goal to use the toolkit for implementation in a broad range of settings (e.g., rural, urban, community, clinical, fitness).

Implementation methods and strategies

Our institutional champion introduced us to and helped us obtain approval from the community partner and provided assistance with grant proposal planning and start-up activities. After receiving funding (National Cancer Institute (NCI); R21CA182601), meetings at the community site focused on leadership buy-in, identifying local champions, and increasing our understanding of the local context. We combined resources from the original efficacy trial (e.g., manual of procedures, education materials) with meeting notes and input from cancer survivors, community/organizational stakeholders, and interventionists to identify important factors to consider when implementing an exercise intervention for rural cancer survivors (7). Using resultant data (7,23,24) and pragmatic experience, we identified several Consolidated Framework for Implementation Research (CFIR) domains (see Fig. 3) as key targets for addressing barriers and leveraging facilitators during implementation (25).

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Figure 3:
Consolidated Framework for Implementation Research domains and subdomains frequently observed during translation of an exercise intervention to a rural community setting; selected barrier and facilitator examples provided to facilitate application.

Major takeaways and challenges

The toolkit consists of a 53-page manual with appendices, PowerPoint presentations (staff training, participant discussion groups), patient education notebook, and 12 training videos for implementation. We observed that our community partner valued their relationship with the academic institution (the originator of the EBI), which facilitated our efforts. We learned that addressing readiness and engagement of local leaders in an ongoing manner and identifying multiple local champions limited project interruption during staff and leadership turn over. Also, logistical limitations (time, money, and capacity) required focusing on the core intervention components. Although we gained critical multilevel stakeholder input, this process was costly, time consuming and required ensuring stakeholders understood the input needed (e.g., creating a shared understanding of the planned intervention). We also found that research-related regulatory requirements (e.g., institutional review board approval) jeopardized feasibility, lengthened the timeline, and conflicted with the community partner’s interest in quicker implementation cycles.

Project 2: The Active Living after Cancer Intervention (Principal Investigator: K.M.B.-E.)

EBI

The Active Living After Cancer (ALAC) intervention teaches cognitive and behavioral skills for increasing physical activity. It is based on the Project Active lifestyle physical activity intervention, which was adapted for breast cancer survivors (26). A randomized trial in breast cancer survivors found that survivors receiving the program demonstrated greater improvements in 6-min walk test performance and physical domains of quality of life than control arm participants (27). The trial and the analysis of program evaluation data from the implementation project described below were both approved by the Institutional Review Board of the University of Texas MD Anderson Cancer Center (protocol nos. BS97-341 and PA16-0398, respectively).

Implementation setting and intended population

We implemented ALAC in the Houston, TX, community, emphasizing delivery to breast cancer survivors who were from minority groups and/or medically underserved (i.e., those who were uninsured, had no personal health care provider, had difficulty accessing health care because of cost, or had low health literacy). Funding was provided by the Cancer Prevention and Research Institute of Texas (CPRIT PP130079). We partnered with Kelsey Research Foundation, a nonprofit arm of a multispecialty clinic, which provided health educators and leveraged their relationships with community organizations to promote the program and identify space for the sessions.

Key implementation questions

This implementation effort focused on EBI adaptation and delivery strategies in a community with minority and medically underserved breast cancer survivors. The EBI primary investigator (K.M.B.-E.) led the adaptation process, guided by the adaptation framework of Escoffery et al. (28) (steps 5–11; (Fig. 4). We reviewed the original intervention to identify the adaptations needed to make the intervention more suitable to a diverse (in education, language, and ethnicity) group of breast cancer survivors. With our community partner, we identified four intervention features needing adaptations: length, cultural relevance and language of materials, staff training, and evaluation format (29).

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Figure 4:
The adaptation of Active Living after Cancer focused on steps 5–11.

Implementation methods and strategies

The program was provided in locations throughout the Houston area, including community centers, nonprofit agencies, a county safety-net hospital, and clinic locations. Over 3 yr, participants (n = 188) reported improvements in physical activity, quality of life, and objective physical functioning (29). We then received additional funding (CPRIT PP170023) to scale-up, expanding ALAC to El Paso, TX, and to survivors of any cancer type. To bridge the geographic distance, we adapted Project ECHO (a telementoring intervention connecting community-based health care providers with specialists) (30) to bimonthly ECHO sessions that provided ongoing training and technical assistance to the health educators. To expand to other cancer types, we included additional cancer site-specific content and images of both men and women. We also made adaptations requested by participants and health educators (e.g., allowing caregivers to participate, incorporating vision boards into goal setting activities). The scale-up phase of ALAC reached over 600 survivors and 90 caregivers, with 40% being monolingual Spanish speakers. Results showed increases in physical activity, quality of life, and physical functioning (31).

Major takeaways and challenges

Intervention adaptation led to simplified and shortened participant materials but maintained key theory-based content and effectiveness. This adapted intervention was effective in improving physical functioning among minority and medically underserved cancer survivors when implemented by community health educators (29). Key characteristics of the outer context were critical to implementation, including established academic/community partnerships and external funding. Adaptation was not a one-time event; adaptations in the intervention and support for health educators continued over two funded projects that lasted 6 yr and included changes to the intended population (including caregivers), training and technical assistance methods (use of Project ECHO), and specific intervention activities and materials to increase relevance. Future directions involve additional adaptations in intervention delivery methods. Additionally, we have increased efforts to document adaptations made by the health educators delivering the intervention with the goal of describing the “adaptome” of ALAC and evaluating the impact of adaptions (32).

Project 3: The Strength after Breast Cancer Intervention (Principal Investigator: K.S.)

EBI

The Strength after Breast Cancer (SABC) intervention (NCI R21-CA152451) was adapted from a progressive resistance exercise intervention proven beneficial for breast cancer survivors in a randomized controlled trial called Physical Activity and Lymphedema (NCI R01-CA106851) (33). The original trial documented benefits of reducing lymphedema flare-ups among breast cancer survivors with lymphedema, reducing onset of lymphedema among survivors with no previous lymphedema diagnosis, and improving physical function, body image, and body composition (33–37). The goal of the intervention was to improve outcomes related to the prevention of lymphedema and/or improvement of lymphedema symptoms. The Physical Activity and Lymphedema and SABC protocols (protocol nos. 803430 and 813176) were both approved by the University of Pennsylvania Institutional Review Board, and all participants provided informed consent before any study activities.

Implementation setting and intended population

Because of community fitness center challenges (e.g., staff turnover, center membership costs, staff training (e.g., unable to complete safety evaluations central to the original intervention), lack of referral connections to cancer treatment centers), the team revised the intervention to be delivered in the setting of outpatient rehabilitation, taught by physical therapists. Our intended population was women diagnosed with breast cancer without regard to timing since diagnosis or diagnosis of breast cancer related lymphedema. Hence, the implementation effort focused on adapting intervention delivery to within the health care setting by physical therapists, with referrals from oncology providers and coverage by third party payers (e.g., Medicare, insurance).

Key implementation questions

We identified champions and key stakeholders in the outpatient rehabilitation and breast center teams to help us identify the following key implementation questions: (a) How do we connect patients to the intervention? (b) How do we ensure someone with appropriate qualifications completed the baseline evaluation? (c) How should we teach the exercises in a way that would promote an ongoing home-based exercise intervention? And (d) how do we get third party payment for the intervention given survivor concerns with cost? We established a total physical therapy session range of 4–8 sessions, leaving the exact number to the discretion of the therapist. The team developed educational materials for the physical therapists, administrators in the outpatient rehabilitation clinic, and clinicians on the breast cancer team.

Implementation methods and strategies

We evaluated the barriers to implementing SABC using the Consolidated Framework for Implementation Research (25,34). Barriers included delivery of the intervention in a group setting (intervention characteristics), payment, eligibility criteria, and referral process. Facilitators included the use of champions and training physical therapists to individualize the intervention to meet the patient’s needs (e.g., one-to-one sessions, adaptations for specific exercises).

We used multiple strategies to address the barriers. We provided ongoing training, given staff turnover, and audited the effectiveness of the electronic medical record (EMR)–based automated referral to SABC. In one clinic, clinicians incorrectly assumed that clicking a box in the EMR for referral prompted a call to the patients from the outpatient rehabilitation clinic. Based on this revelation, the EMR was revised to function as the clinicians expected, which increased enrollment from 39% (prerevision) to 65% (postrevision).

Major takeaways and challenges

The primary takeaway from the implementation of the SABC program in the health care setting is that a toolkit, champions, and technical assistance are crucial to success. The SABC program is still covered by third party payers, the toolkit has been commercialized as a Web-based training, and SABC is offered in over 1000 locations across the United States and beyond (38). A consistent, ongoing challenge is getting oncologists to refer patients into the program.

Using the EPIS Framework to Map Out Implementation Strategies

As shown in Fig. 2, 27 strategies were used across the different EPIS phases, of which two (access new funding and develop educational materials) were reused from the previous phases with a different operational definition in the sustainment phase. The specific numbers of strategies varied between the three implementation efforts (BEAT Cancer used 17 strategies, ALAC used 21 strategies, and SABC used all 27 strategies). Our examples used strategies from all nine overarching categories that map out the 73 discrete strategies in the second phase of the ERIC study (see Supplemental Content, https://links.lww.com/TJACSM/A193) (18).

DISCUSSION

Implementation efforts were iterative and nonlinear, turning to different strategies and adaptations as obstacles were identified. Given the limited literature on the implementation of exercise oncology EBIs, this article presents important practice-based evidence and data for promoting future implementation and intervention research. With regard to context, the YMCA and other community fitness centers have been reported as feasible implementation settings for cancer survivors on and off cancer treatment (39–41). This is not the experience with SABC because implementation in community fitness centers was abandoned because of clinical conditions being treated, cost, and staff turnover. This is consistent with the need for properly trained fitness professionals when translating programs that deliver more structured, prescriptive exercise progression outside the research setting. In contrast, ALAC, which focuses more on encouraging lifestyle physical activity (rather than a structured exercise approach), has successfully scaled up to several community locations that are not fitness centers. With regard to the “how” of implementation, Pinto et al. (42) reported successfully training peer coaches to complete an evidence-based telephone intervention, similar to ALAC’s promising use of Project ECHO to provide ongoing training to intervention personnel.

The challenge of funding was a common theme across implementation efforts. However, new payment models in health care that incentivize outcomes and quality may lead more health care systems to support interventions that can improve cancer survivors’ physical functioning (43). Additionally, as survivors become more aware of the exercise benefits, oncology practices may view these interventions as a marketing tool and thus be willing to absorb intervention costs. Also, payment models may differ based on the type of intervention (e.g., a program similar to SABC might be provider based, whereas maintenance or self-directed programs might be fee based). Further, funding challenges may differ in countries with socialized health care or limited resources to invest in the health care system.

Research to identify optimal implementation strategies is currently missing from the published literature but has been promoted as an important next step in the field of implementation science (44). Our systematic approach to compiling strategies across the implementation efforts presented in this article align with calls in the field to improve the tracking and reporting of implementation strategies (19). Although several publications report on interventions implemented in nonresearch settings, few have described the challenges faced, iterative process of adapting throughout the translation process, and implementation strategies used (45–47). Hence, our contextual description of implementation within the realities of the real world is a potential starting point for future exercise oncology implementation science research and application. The efforts described here used strategies from all nine overarching categories that map on to the 73 discrete strategies in the second phase of the ERIC study (18), including using evaluative and iterative strategies, providing interactive assistance, adapting and tailoring to context, developing stakeholder interrelationships, training and educating stakeholders, supporting clinicians, engaging consumers, utilizing financial strategies, and changing infrastructure (see Supplemental Content, https://links.lww.com/TJACSM/A193).

Limitations

The validity of our observations is supported by consistency with ERIC strategies and frequent overlap in strategies used despite the diversity of the EBIs described. We do, however, acknowledge important study limitations. First, our experience is only limited to that of the United States and may not be generalizable to countries with different cultures or health care payer systems. Also, our projects were not designed to rigorously measure, assess, or quantify the effects of the strategies used, and as such, our data can only be used to generate hypotheses warranting further study.

Conclusions

Implementing exercise oncology EBIs in nonresearch settings can be iterative and challenging and requires strategies that target implementation barriers and facilitators. Our examples highlight implementation strategies relevant to exercise oncology EBIs and the need for future research to determine the optimal combination and timing of strategies used. These future research directions should include a focus on how to choose and engage champions, deal with cost concerns, increase readiness for dealing with a clinical population with diverse and unique needs, and engage the cancer survivor in the EBI.

The authors acknowledge the efforts of the research teams, clinicians, and community partners who led and supported the implementation efforts described in this report. Additionally, they thank the participants in the projects mentioned in this article for their time and insights contributing to the research.

The authors declare no conflicts of interest. Funding for Project 1: National Cancer Institute R21CA182601. Funding for Project 2: National Cancer Institute R21CA89519; CPRIT PP130079; CPRIT PP170023; CPRIT PP200028. Funding for Project 3: National Cancer Institute R01CA106851 and R21CA152451.

The results described in this article do not constitute endorsement by the American College of Sports Medicine.

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