Translating Evidence from Dutch Exercise Oncology Trials in Patients with Breast Cancer into Clinical Practice Using the RE-AIM Framework

Ten Tusscher, Marieke R.; Stuiver, Martijn M.; Kampshoff, Caroline S.; Huijsmans, Rosalie J.; Aaronson, Neil K.; Velthuis, Miranda; Gal, Roxanne; Van Waart, Hanna; May, Anne M.; Buffart, Laurien M.

doi:https://doi.org/10.1155/2023/2296881

European Journal of Cancer Care

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Abstract Introduction Methods Results Discussion Conclusion Data Availability Conflicts of Interest Authors’ Contributions References Copyright Related Articles

Research Article | Open Access

Volume 2023 | Article ID 2296881 | https://doi.org/10.1155/2023/2296881

Translating Evidence from Dutch Exercise Oncology Trials in Patients with Breast Cancer into Clinical Practice Using the RE-AIM Framework

Marieke R. Ten Tusscher,¹Martijn M. Stuiver,^2,3,4Caroline S. Kampshoff,⁵Rosalie J. Huijsmans,⁶Neil K. Aaronson,²Miranda Velthuis,⁷Roxanne Gal,⁸Hanna Van Waart,^9,10Anne M. May,¹¹and Laurien M. Buffart¹

Academic Editor: Kevin Sheng-Kai Ma

Received30 Mar 2023

Revised18 Jul 2023

Accepted01 Sept 2023

Published10 Nov 2023

Abstract

Purpose. We aimed to evaluate the potential for implementing exercise interventions for patients with breast cancer in the Netherlands, based on findings of the Dutch randomized controlled trials in this population. Methods. We evaluated the implementation of four Dutch exercise trials retrospectively, using the five dimensions of the RE-AIM framework: Reach (exercise participation rate), Effectiveness for physical fitness, fatigue, quality of life, and physical function, Adoption (e.g., satisfaction of physical therapists guiding the exercise intervention), Implementation (cost-effectiveness and exercise adherence correlates thereof), and Maintenance (maintenance of exercise levels by individual patients and sustainability of exercise delivery at organization level). Thereby, we reflect on these results using (international) literature to gain better insight in overall barriers, facilitators, and opportunities for further implementation of exercise interventions. Results. Participation rates of 44–52% not only indicated acceptable Reach in the context of a trial but also indicated room for improvement. Effectiveness of exercise during and after treatment was demonstrated in most trials showing benefits for aerobic fitness, physical fatigue, quality of life and physical function, and high patient satisfaction. Adoption of the exercise interventions by physical therapists was adequate (satisfaction score: 7.5 out of 10). Evaluation of Implementation indicated adequate adherence to supervised exercise, inconsistent findings on potential correlates of adherence, and promising results on cost-effectiveness. Currently, reimbursement for exercise programs is lacking. Maintenance of intervention effects at the patient level was limited and inconsistent. Maintenance of intervention availability at the organizational level was facilitated by an extensive network of specially trained physical therapists, but better communication and collaboration between different healthcare professionals are desired. Conclusions. Improved implementation could particularly be achieved by increasing reach and improved focus on exercise maintenance on both the patient and organizational level.

1. Introduction

Evidence from randomized controlled trials (RCTs) indicates that exercise benefits aerobic fitness [1], fatigue [2], health-related quality of life (HRQoL) [3], and physical function [3, 4], during and after cancer treatment. This has led to the development of national and international guidelines [5–9] recommending exercise as an integral part of cancer care in a number of countries and professions, including sports medicine [4], medical oncology [10], and physical therapy [11, 12]. However, widespread implementation of exercise interventions is still limited. Translating research from RCTs into practice has shown to be difficult because of problems with population representativeness, limited (financial) resources, and program availability and sustainability [13].

In 1999, the RE-AIM framework was developed to evaluate the potential for dissemination of research into clinical practice and to facilitate this process [14]. Since then, RE-AIM has been used to plan, evaluate, and review health promotion and disease management interventions [14, 15]. In the RE-AIM framework, the overall impact of an intervention is described in five dimensions: reach, effectiveness, adoption, implementation, and maintenance (Table 1).

Over the past years, four exercise RCTs have been conducted in the Netherlands that evaluate the effect of supervised exercise interventions on aerobic fitness or fatigue as primary endpoint in patients with breast cancer during treatment (physical activity during cancer treatment (PACT) [16–21] and physical exercise during adjuvant chemotherapy effectiveness study (PACES) [22–26]) and after treatment (resistance and endurance exercise after chemotherapy (REACT) [27–30] and UMBRELLA Fit [31, 32]) (Table 2).

In this study, we aimed to evaluate the potential for implementation of exercise interventions for people who have been treated for breast cancer with curative intent, based on these four RCTs, with the use of the RE-AIM framework. We summarize the findings from the four Dutch trials only, since implementation of interventions is a dynamic, context-specific process [33], with (country) specific and more generalizable components. In addition, we reflect on these results using (international) literature (e.g., trials and reviews) to gain better insight in overall barriers and facilitators for the implementation of exercise interventions. Finally, we describe opportunities for further optimization of implementation.

2. Methods

For each dimension of the RE-AIM model, we summarized the findings from the four Dutch trials, as published before August 2022, using the operationalizations of reach, effectiveness, adoption, implementation, and maintenance described in Table 1. Most results have been published previously [17, 19, 20, 22, 23, 25, 26, 32], except for information on patient satisfaction (PACT and UMBRELLA Fit trial). As the REACT trial also included patients with other types of cancer, we performed subgroup analyses on the subpopulation of patients with breast cancer, except for the cost-effectiveness analyses of which results are presented from the original papers. For better comparisons, we calculated Cohen’s d effect sizes (ES) of the intervention effects, where significant effects () were considered as no substantial difference for ES ≤ 0.2, small for ES 0.2–0.5, moderate for ES 0.5–0.8, and large for ES ≥ 0.8 [34].

3. Results

3.1. Reach

3.1.1. Summary of Results of Dutch RCTs

Across the four RCTs, 44–52% of eligible patients were willing to participate in the trials and the exercise intervention. Main reasons for nonparticipation were lack of time, mental burden, travel distance to the hospital, not wanting to be randomized, or wanting to exercise on their own (Table 3).

Comparison of participants and nonparticipants indicated that patients with a higher educational level were more likely to participate in exercise trials both during and after treatment (Table 3). Additionally, behavioral motivational factors were associated with participation during chemotherapy. Patients with more expected benefits of exercise, higher self-efficacy, fewer negative attitudes, more social support, and fewer perceived barriers to exercise were more likely to participate. Conversely, for exercise interventions following completion of anticancer treatment, patients who perceived more barriers were more likely to participate (Table 3).

3.1.2. Reflections and Opportunities to Improve Implementation

The reported participation rate of 44–52% in the Dutch exercise trials is somewhat higher than the pooled estimate of 30% reported in a meta-analysis of 23 exercise trials in patients with breast cancer [35]. The highest participation rate of 52%, reported by the UMBRELLA Fit trial, is likely related to the trials within cohorts (TwiCs) design, in which patients participating in an observational cohort were randomly invited to participate in an exercise intervention, thereby limiting intervention nonparticipation due to unwillingness to be randomized [31, 36]. In other trials, this proportion was shown to be approximately 10–15% [17, 26] (Table 3). Additionally, participation rates were influenced to some extent by the eligibility criteria employed, as they most often excluded patients with severe comorbidities and those with cognitive disorders or not fluent in Dutch. These patients may benefit even more from exercise guidance, as they may need specific exercise prescriptions, and may be less aware of health benefits and less able to find adequate health information, respectively. Patients with insufficient mastery of the language may benefit from additional health communication strategies, such as including visual aids to improve reach [37, 38].

The finding that travel time to the hospital was a commonly reported barrier to exercise participation is in line with other studies reporting that cancer survivors rated long travel time to exercise facilities as an important barrier to participation, particularly when supervised sessions were scheduled for 2 or 3 times per week [39, 40]. Travel time can be reduced by offering exercise interventions in local physical therapy practices or in the community settings close to patients’ homes. In the Netherlands, regional networks of physical therapists working with patients with cancer are expanding, facilitating the accessibility to supervised exercise sessions. In addition, a network of fitness instructors with additional oncology education is developing, which might ease the transition from healthcare to community settings.

Experiencing less “barriers to exercise” was associated with higher participation during chemotherapy, while, after treatment, patients with more barriers were more likely to participate. These findings might indicate that at start of treatment, patients might be too occupied with the burden of diagnosis and treatment to overcome existing barriers to exercise, while, after treatment, patients’ declined fitness levels and difficulties overcoming these might make them more prone to accept exercise guidance.

Two other commonly reported barriers are time and mental burden (e.g., “having too many things on one’s mind”) [41]. In studies with patients under active treatment, the timing of trial inclusion before the start of chemotherapy is challenging because of the short time window between diagnosis and start of treatment and because patients who were diagnosed recently can be overwhelmed [26]. These barriers might be reduced by improving knowledge on the content and benefits of exercise during and after chemotherapy and by optimizing the timing of discussing exercise with patients. Shaping knowledge is among the most commonly used behavioral change techniques [42]. Specifically, instructions on how to perform the exercise behavior and information on the health consequences thereof were often part of interventions that were effective in improving exercise behavior in breast cancer survivors [43]. Hence, increasing knowledge of health benefits may help patients to restructure priorities. This may also be the case for patients with lower educational levels, who were less willing to participate in exercise trials both during and after chemotherapy [26, 30]. However, for the latter patients, the educational techniques applied might need to be adapted, for example, by breaking down information into small concrete steps and/or by including visual aids [37].

In the Netherlands, an e-learning module is available for nurse (practitioners), which, in addition to addressing common effects of exercise in patients with cancer, also pays attention to how to coach and motivate patients towards improving and maintaining adequate exercise levels [44]. The optimal timing of discussing exercise with patients is unknown while results from the Dutch trials indicated that thinking about exercise shortly after diagnosis may be an additional burden for some patients; for other patients, the diagnosis may be a teachable moment [45] and the right time to discuss exercise at the time of diagnosis [46]. It is also likely that patients’ information needs and receptivity change over the course of their treatment and recovery although this is currently an understudied subject. The ACSM’s Exercise Is Medicine (EIM) initiative proposes assessing, advising, and referring to physical activity in a recurrent pattern to take into account the different preferences and changing needs of patients for referral to exercise programs [47]. For trial purposes, with small windows of opportunity for including patients at the start of chemotherapy, an improvement in research infrastructure and a proactive approach to patients would be helpful, e.g., an outpatient research clinic, where patients are being asked at diagnosis for a broad consent for being approached for (future) research participation. Broad consent enables researchers to directly approach patients without intercession of a healthcare provider and outside a medical appointment.

Physicians play an important role in referring patients to exercise, and thus, in increasing the reach, as patients are more likely to participate in exercise, it has been recommended by a physician [40, 48, 49]. However, while most oncologists, including those in the Netherlands, report understanding the importance of exercise, only one in three actually refers patients [50–52]. Reported barriers for this poor referral rate are lack of time, insufficient knowledge, and safety concerns [53]. It has been suggested that the development of a roadmap for oncology clinicians with detailed pathways for exercise programming, in which discussing exercise participation becomes part of routine care, would facilitate referral [47]. However, empirical evidence on the effectiveness of such a roadmap and feasibility in Dutch clinical practice is lacking. Additionally, physicians’ referral may also be improved by increasing patient awareness of exercise benefits, empowering patients to raise the issue of referral themselves during consultation [54], and improving insurance reimbursement and thereby accessibility [52].

3.2. Effectiveness

3.2.1. Summary of Results of Dutch RCTs

Supervised exercise interventions during chemotherapy had a significant positive effect on aerobic fitness in one study [23], but it was not statistically significant in the other [17]. Supervised exercise limited physical fatigue significantly, while an unsupervised exercise program did not (Table 3). Both supervised and unsupervised exercise had a significant beneficial effect on physical functioning in one trial [23] but not in the other [17] (Table 3).

Exercise after completion of treatment significantly improved aerobic fitness, physical functioning, global QoL, and general fatigue in one trial (Table 3) and physical fatigue in both trials [32] (Table 3).

Average patient satisfaction was 8.5 (on a 1–10 scale) for supervised exercise during chemotherapy, 8.4 for supervised exercise after treatment, and 7.4 for an unsupervised exercise program during chemotherapy. Up to 25% of patients reported that the exercise program during chemotherapy was “too burdensome.” After treatment, up to 16% of patients reported the program as “not being tailored enough,” up to 10% reported difficulties with scheduling exercise sessions, and some patients reported the exercise program as “(too) heavy or exhausting” (12% up to 17% for patients in the High Intensity (HI) exercise group) (Table 3).

3.2.2. Reflections and Opportunities for Further Implementation

The beneficial effects of exercise on aerobic fitness, fatigue, and HRQoL found in the Dutch trials correspond with findings from other studies [4]. Of note, the stringent eligibility criteria of RCTs (e.g., excluding patients with serious orthopedic and cardiovascular or pulmonary comorbidities) may hamper generalizability of the beneficial effects to all patients with breast cancer treated with curative intent. Although it may be expected that these patients could also benefit from exercise, more extensive tailoring of the exercise protocols is likely necessary to take specific comorbidities into consideration [55].

The beneficial effects on aerobic fitness, fatigue, and HRQoL, both during and after treatment, were also reported by several meta-analyses on aggregated and individual patient data (IPD) meta-analyses [1–3] that also reported larger benefits for supervised interventions and patients with lower baseline HRQoL [56]. High baseline values of HRQoL may explain the lack of effects on HRQoL in the UMBRELLA Fit trial as the HRQoL in this cohort of patients was already comparable to the Dutch general female population at the start of the intervention, leaving little room for improvement [32].

The average effects of exercise on aerobic fitness observed in the Dutch trials correspond to the mean peakVO₂ improvements of 1.80 and 2.13 ml/kg/min reported in the literature [57]. Strikingly, previous studies with IPD analyses reported that exercise interventions during treatment did not yield benefits for aerobic fitness in patients with a low fitness level (peakVO₂ below 15.4 ml/kg/min, which is the threshold for functional independence in women [58]) at baseline [56]. Also, effects on aerobic fitness were smaller in older patients [1]. The limited effects in these subgroups may be related to low adherence or inability to complete exercises as intended and highlight the need for exercise interventions that are specifically tailored to older and unfit cancer patients to further improve implementation.

The Dutch trial results suggest a dose-response effect for exercise intensity on aerobic fitness (low-to-moderate (LMI) versus HI) (Table 3). Internationally, in the past 5 years, an increasing number of studies successfully examined the effects of high intensity interval training (HIIT) in patients with cancer and found positive results on cardiorespiratory fitness and cancer-related fatigue [59, 60]. However, results of the Dutch trials suggest that HIIT may not be the best choice for all patients, as up to one quarter of the patients indicated that the exercise intervention conducted during cancer treatment was too burdensome directly after their chemotherapy administration, and 17% of those who participated in HI exercise after cancer treatment found it (too) heavy or exhausting (Table 3). Also, depending on the goal of the intervention, higher exercise intensity may not always be necessary. For example, relatively low volumes of resistance exercises, at moderate-to-high intensity, have been found to yield significant benefits in terms of fatigue levels and HRQoL in patients with prostate cancer [61].

Despite the finding that some patients found the intervention to be too strenuous or burdensome, the vast majority of the patients in the four Dutch trials indicated being very satisfied with the exercise interventions in which they participated. This has also been the case in other exercise trials in patients with breast cancer [62–64]. Patients in the Dutch trials suggested that they would appreciate being able to reschedule missed exercise sessions, add more variety to the prescribed exercises, and combine the exercise sessions with yoga [22]. This was also found in a study of women with ovarian cancer [65]. Taking patient preferences into account can increase enjoyment, which, in turn, can have a beneficial effect on exercise maintenance [66]. At the same time, to achieve their goals and the desired health benefits, it is important that patients are informed on the exercise frequency, intensity, type, and time (FITT) required. Patient satisfaction, and thereby potentially exercise maintenance, can be further improved by taking sufficient time for exercise familiarisation, optimizing exercise scheduling in relation to chemotherapy administrations [67], and adequate tailoring of exercise intensity to the individual’s fitness level.

The generally lower level of satisfaction reported for the home-based exercise counselling compared to supervised exercise may be related to the limited time devoted by healthcare professionals (e.g., physical therapists or nurse practitioners) (HCPs) to instructing and motivating patients and to individualizing the home-based exercises. Motivational interviewing appeared to be an effective technique to improve exercise behavior of patients with cancer in some studies [68, 69], but not all [70]. Dedicated time, and better training in exercise counselling, and development of supportive tools may improve the counselling skills of HCPs delivering exercise programs.

3.3. Adoption

3.3.1. Summary of Results of Dutch RCTs

Most patients in the Dutch RCTs were recruited from both community and university hospitals and were referred to a physical therapist specifically trained to work with patients with cancer, located close to the patients’ homes. The physical therapists who delivered the intervention after completion of cancer treatment were generally satisfied with the content of the trial intervention (supervised aerobic and resistance exercise two days per week, supplemented by counseling on unsupervised exercise for three other days). The average satisfaction score was 7.5 (on a 1–10 scale, Table 3). While, overall, the physical therapists were satisfied with the exercise intervention, some reported that they would have preferred to prescribe more variation in the resistance exercises (20%) that the exercise counseling was too time-consuming (20%) and that physical therapists could benefit from some additional training in this regard (10%) (Table 3).

3.3.2. Reflections and Opportunities to Improve Adoption

Few studies have described experiences of professionals delivering exercise interventions to patients with cancer treated with curative intent in the context of a trial. More variation in exercises has also been suggested by other studies, in order to prevent boredom, better tailor exercises to patients’ preferences, needs (e.g., functional training), or capabilities, and to add exercise types other than resistance or aerobic exercises, such as balance exercises [65, 71]. In addition, physical therapists and personal trainers have reported that guidance of a group of patients can be challenging (e.g., dealing with different types of group dynamics; providing sufficient attention to individual patients’ abilities and needs) [72, 73]. This indicates the importance of qualified trainers and preferably small group sizes although the latter needs to be balanced with affordability.

Results of focus groups in various HCPs working in primary or secondary care in the Netherlands (e.g., physicians, nurses, and physical therapists) reported that insufficient evidence about benefits of exercise programs was a barrier for their use [71]. This can be a reason for not referring patients to exercise programs. Hence, efforts to disseminate the evidence on the effects of exercise on cancer outcomes will likely accelerate the implementation of exercise as part of standard cancer care [74]. Additionally, these exercise programs should be adequately tailored to the individual patients’ needs, capabilities, and preferences [71] while taking evidence-based exercise frequency, intensity, type, and time (FITT) into account.

3.4. Implementation

Implementation was evaluated based on (a) exercise adherence and (b) resources and intervention costs [75].

3.4.1. Exercise Adherence

(1) Summary of Results of Dutch RCTs. The median attendance rates of supervised exercise in the Dutch trials varied between 77% and 98% and were 71% for unsupervised exercise (Table 3). Median compliance rates ranged between 81% and 88% for moderate intensity aerobic exercises, between 50% and 87% for HI aerobic exercises, and between 84% and 94% for resistance exercises (Table 3). The most frequently reported reasons for not attending the sessions during chemotherapy were feeling too ill (53%) and logistical reasons (30%). During chemotherapy, higher disease stage, having a partner, higher educational level, and a lower body mass index (BMI) were significantly associated with better attendance [20, 22]. Results on predictors of compliance to the prescribed exercises during and after treatment suggested a difference between exercise type (resistance versus aerobic), intensity (LMI versus HI), and delivery mode (supervised versus unsupervised) [20]. In general, after cancer treatment, psychosocial factors, such as higher self-efficacy and having a more positive attitude towards exercise, were associated with a higher attendance and compliance to HI but not to LMI exercise (Table 3).

(2) Reflections and Opportunities to Improve Implementation. The exercise adherence rates and the diversity in predictors of adherence in Dutch studies are in line with previous findings from other studies [76–78]. This diversity can be explained by differences in exercise prescriptions between studies and in the predictors studied. The finding that treatment-related adverse effects (“feeling too ill”) accounted for over half of the total missed sessions is also in line with other exercise studies in patients with breast cancer receiving chemotherapy [79, 80]. Consideration of side effects as part of exercise program design has been proposed, for example, by using “chemotherapy-periodized” exercise prescriptions that take chemotherapy side effects into account [67]. The finding that patients with lower exercise self-efficacy and more negative attitudes towards exercise had more difficulties with adhering to HI exercise suggests that realistic goal setting and starting at a lower intensity, to gain confidence before progressing to HI exercise, may be useful to improve adherence of these patients.

Previous systematic literature reviews found exercise history to be associated with better exercise adherence [77, 78]. This was not supported by the results from the Dutch trials, which suggests that other factors may be more important. It should be noted that the overall adherence reported in the Dutch trials was relatively high. This may not, however, turn out to be the case in clinical practice, due to variation in motivation and less emphasis on required adherence [73, 81]. Future studies in daily clinical practice that yield real-world data on exercise adherence, collected via electronic medical records, might help elucidate which factors are associated significantly with adherence to exercise outside the trial context and to identify subgroups of patients and cancer survivors that might require adjustments to the exercise intervention or psychosocial and behavioral support for improving adherence.

3.4.2. Resources and Intervention Costs

(1) Summary of Results of Dutch RCTs. Two of the Dutch trials assessed the cost-effectiveness of the exercise interventions during treatment. In one trial, the supervised exercise intervention during chemotherapy was found to be cost-effective with a probability of 45% at a willingness-to-pay of 20.000€/quality-adjusted life year (QALY) [25]. The other trial reported that, at a willingness-to-pay of 20.000€/QALY, the probability that the intervention would be cost-effective was very low (2%) [21]. The unsupervised exercise intervention was not cost-effective (25% probability for cost-effectiveness at a willingness-to-pay of 20.000€/QALY). After completion of chemotherapy, a HI-exercise program was more cost-effective than a LMI exercise program [29], with a probability of 91% at a willingness-to-pay of 20.000€/QALY.

(2) Reflections and Opportunities for Further Implementation. Results on the cost-effectiveness of exercise interventions in Dutch trials were mixed, possibly explained by contamination or differences in follow-up time [21, 25]. Previous systematic reviews showed that supervised exercise interventions and multimodal interventions were cost-effective when they yielded significant beneficial effects on health outcomes such as energy, fear of recurrence, mood, and pain [82, 83].

In the Netherlands, exercise supervision from a physical therapist is currently not reimbursed by basic healthcare insurance. However, exercise sessions for patients who have had surgery prior to their chemotherapy or received radiotherapy treatment in the past 6 months can be reimbursed from the 21st session onwards until 1 to 2 years (depending on the treatment and insurance). Additionally, biweekly one-hour supervised exercise sessions can only be provided in group sessions of 2–10 persons because physical therapists are allowed to invoice for a maximum of 30 minutes per day per person. Fortunately, group sessions are often appreciated by cancer survivors and facilitate peer support [22, 62, 65] and may consequently improve adherence rates. On the other hand, group sessions are often less flexible with regard to exercise times, which has been reported as barrier to (adhering to) exercise programs [22]. Also, group sessions are not suitable for every patient as some patients feel uncomfortable with group exercise and/or may require more intensive coaching than possible in group settings.

More information on the cost-effectiveness of exercise interventions and consideration of other healthcare reimbursement strategies (e.g., bundled-payment models) could be helpful to better inform discussions among health policy-makers and insurers about appropriate reimbursement policy and insurance coverage for exercise interventions during and after chemotherapy. Future cost-effectiveness evaluations need to take into account that higher chemotherapy completion rates resulting from exercise interventions may result in higher costs of medication and secondary healthcare but also higher survival rates [84] and that work absenteeism may be underestimated when absence, beyond the percentage sick leave that is agreed upon by patients and employers, is not reported as absenteeism days [25].

3.5. Maintenance

In this section, we evaluated maintenance at the patient level¸ describing long-term effects of the intervention, and at the organizational level, describing the extent to which the exercise programs have been institutionalized and integrated into routine practice, as well as the policies enabling program sustainability.

3.5.1. Patient Level

(1) Summary of Results of Dutch RCTs. Exercise during chemotherapy did not yield significant effects on aerobic fitness, self-reported fatigue, or HRQoL at follow-up (i.e., 6, 8, and 48 months) [19, 23]. However, patients who participated in an exercise program after completing their oncological treatment successfully maintained their improved levels of cardiorespiratory fitness and HRQoL at one-year postintervention (Table 3). The positive intervention effects on HRQoL observed at one-year follow-up were significantly larger for HI compared to LMI exercise (Table 3).

(2) Reflections and Opportunities for Improving Maintenance at the Patient Level. The limited maintenance of intervention effects on most outcomes might be explained by the uptake of exercise by control group participants after the completion of chemotherapy or the specific focus on improving outcomes during the intervention period without sufficient incorporation of behavioral change techniques to maintain healthy behaviors in the long term.

Sustained benefits on aerobic fitness were found one year after completion of exercise interventions and after cancer treatment. Nevertheless, peakVO₂ levels were still “poor,” as compared to healthy adults [29]. This might indicate that a 12-week program might be too short for patients to fully return to normative values, and patients may not have received sufficient guidance to continue exercising at home at sufficient intensities after completion of the trial to continue improving their peakVO₂. This is in line with the previously mentioned feedback of physical therapists that they had insufficient time for counseling and expressed a need for additional education (Table 3). Further development of tools to improve the quality of counseling and efficient integration into daily practice might improve maintenance of adequate exercise levels to further improve peakVO₂. This could be achieved by improved incorporation of behavioral change techniques, such as “instruction on how to perform the behavior,” “feedback and self-monitoring of behavior,” and “goal-setting (behavior)” [43]. Education on how to use behavior change techniques may help to overcome some perceived barriers of exercise maintenance that have been reported by patients with breast cancer, including psychological barriers (e.g., lack of motivation, fears, dislike of gym, or not being the “sporty type”), physical barriers (e.g., ageing, side effects of cancer treatment, and other comorbidities, weight gain), and contextual and environmental barriers (related to employment, traditional female care-giving roles, access to facilities, and seasonal weather) [85].

3.5.2. Organizational Level

(1) Summary of Results of Dutch RCTs. For the conduct of the Dutch trials, physical therapists were trained to supervise patients with cancer in exercising during chemotherapy and after treatment, within the initiated Onconet network. After trial completion, the Onconet foundation further educated physical therapists on the content and delivery of exercise programs for patients with cancer, and thereby consolidated and expanded a physical therapist network. The education also includes mandatory refresher courses where physical therapists are updated on results from recent studies. Currently, the network of physical therapists specialized in guiding patients with cancer is nationwide, with over 700 locations mostly within a 15-minute travel distance from any address. Additionally, MSc-level programs are available to educate physical therapists in oncology.

(2) Reflections and Opportunities for Improving Maintenance at the Organizational Level. In the Netherlands, currently, most supervised exercise interventions are offered by allied healthcare professionals. In primary care, this is primarily via physical therapists working in private clinics. Exercise can also be offered as part of a multidisciplinary rehabilitation program in secondary (hospitals) or tertiary (rehabilitation clinics) care. Outside of the healthcare system, fitness trainers with oncology specialization are increasingly available. These fitness professionals mainly deliver exercise interventions to patients who have completed treatment at least 3 months earlier [71].

Results from a qualitative study in the Netherlands indicate that HCPs working in primary care (e.g., general practitioners, physical therapists) perceive collaboration, communication, and referral between primary and secondary HCPs to be suboptimal [71], whereas HCPs working in secondary care (e.g., physicians, nurses, and paramedics) raised general concerns about inadequate cooperation and networks between healthcare institutes [71]. The HCPs suggested that more use of health information technology, improved access to electronic health records, improved rehabilitation guidelines with recommendations about roles and responsibilities of each HCP, and better networks would improve the implementation of exercise in cancer care [71].

Internationally, the most reported barriers to integrating exercise in oncology settings are at the organizational level [86]. These barriers are related to the limited capacity and resources of staff, including insufficient time to prescribe and refer patients to exercise programs, and to the organization of care processes (e.g., absence of an established care pathway or structure) [86]. To reduce organizational barriers in the Netherlands, the “Taskforce Cancer Survivorship Care” has been established since 2017. In this taskforce, HCPs, policymakers, researchers, and patient organizations join forces aiming to improve attention for and optimization of quality of care over the whole cancer continuum and to improve organizational structures by better coordination between HCPs [87]. The taskforce also pursues an increase of physical therapist participation in multidisciplinary and oncology care networks, enabling further knowledge exchange and improved communication with other HCPs.

4. Discussion

In this study, we have used the RE-AIM framework to describe the potential for implementation of exercise interventions for patients with breast cancer, based on four RCTs previously conducted in the Netherlands. Results from these RCTs demonstrated that exercise during and after treatment has beneficial effects on aerobic fitness, fatigue, and HRQoL in patients with breast cancer. Additionally, both patients and physical therapists were generally satisfied with the intervention, but there were challenges to exercise maintenance.

The current network of physical therapists specialized in oncology that was initiated at the start of the trials continues to expand and represents a fruitful interaction between research and clinical practice. The current evaluation revealed key opportunities to further optimize implementation of exercise programs in the oncology setting. First, there is room to further increase knowledge and awareness among HCPs of the potential benefits of exercise and to improve organizational structures to increase referral to supervised programs. Improving awareness and referral requires more insight into perspectives of organizational stakeholders and policymakers and optimal dissemination of patient information between HCPs for which a whole system approach is needed [71, 86].

Second, although the interventions in the Dutch exercise trials were tailored to individuals’ fitness level and treatment side effects, specific subgroups of patients, such as the elderly and those who are in poor physical condition, are more prone to nonparticipation and appear not to benefit as much [1, 56]. These patients may benefit from an even more personalized and goal-directed functional exercise training program. Such programs have been shown to be feasible and promising in patients with metastatic breast cancer [88]. Similarly, a patient-centred, goal-directed, self-management enhancing functional exercise program that is based on a biopsychosocial model, Coach2move, has shown to be (cost-)effective in improving physical activity and function in community dwelling older adults with mobility problems [89]. A personalized program that is tailored to the individual’s needs and preferences, including behavioral change techniques such as “goal-setting” and “feedback and self-monitoring of behavior,” may also facilitate sustained benefits over time. Successful inclusion of behavioral change techniques as part of exercise supervision may require additional schooling for physical therapists.

Finally, the implementation of exercise programs for all patients with cancer is currently hampered by the lack of reimbursement of physical therapist-guided exercise programs during and after treatment. The Taskforce Cancer Survivorship aims to improve healthcare during and after cancer treatment, and one of the pillars of the Taskforce is to improve reimbursement of allied healthcare [87].

Some limitations of our study should be noted. Because it has been suggested that implementation strategies must be tailored to its context to improve effectiveness [90], we summarized exercise trials with a homogeneity in settings, circumstances, and conditions, thereby specifically focusing on patients with breast cancer in the Netherlands. Hence, caution is needed when generalizing our findings to other countries with different healthcare systems and to patients with other cancer types or advanced cancer [91, 92]. On the other hand, the findings from Dutch trials seem to echo those of studies conducted in other countries. Additionally, we based our assessments on a retrospective evaluation of the potential impact of exercise intervention trials. Our findings might have been different if data from the clinical practice setting had been collected prospectively (e.g., information on treatment referral and treatment fidelity outside of the context of a trial). Future studies should, therefore, prospectively evaluate the implementation of exercise interventions using the RE-AIM framework, for example, by collecting real-world data to describe characteristics of patients who are referred to exercise interventions and to register the delivered exercise prescription in terms of FITT-factors and the resulting changes in aerobic fitness, physical functioning, HRQoL, and achievement of physical therapy goals. This would also facilitate obtaining information about and from patients with comorbidities or those who otherwise would be excluded from trials or referred to less extent to trials [93, 94]. Such collection of real-world data would be facilitated by an adequate registration system to structurally monitor clinical practice, in order to learn from every patient, and subsequently optimize healthcare [95]. Moreover, future research could benefit from hybrid designs, in which elements of clinical effectiveness and implementation research are combined [73, 96]. This might speed up the translation of research’s finding into clinical practice 97.

5. Conclusion

The RE-AIM framework facilitated a retrospective evaluation of the impact of exercise interventions and their potential for implementation in clinical practice. We found acceptable RE-AIM outcomes in terms of participation rates, intervention effects, satisfaction of patients and physical therapists, and adherences rates within the trial context. Additionally, an established network of physical therapists educated in oncology facilitates the maintenance of exercise interventions outside of clinical trials. We have recommended several steps that could be taken to further improve implementation of exercise programs for cancer patients and survivors, including improved referral (reach), improved tailoring of exercise interventions to individual needs and preferences, improved attention to maintenance of exercise behavior (effectiveness, adoption, implementation, and maintenance), and improved reimbursement (reach and maintenance).

Data Availability

Data presented in this trial are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Authors’ Contributions

All authors contributed to the study conception and design. Marieke R. Ten Tusscher, Laurien M. Buffart, Caroline S. Kampshoff, Hanna Van Waart, and Roxanne Gal collected the aggregate data. Marieke R. Ten Tusscher and Laurien M. Buffart performed additional subgroup analysis. Marieke R. Ten Tusscher and Laurien M. Buffart wrote the first draft of the manuscript. Martijn M. Stuiver, Caroline S. Kampshoff, Rosalie J. Huijsmans, Neil K. Aaronson, Miranda Velthuis, Roxanne Gal, Hanna Van Waart, and Anne M. May commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Copyright © 2023 Marieke R. Ten Tusscher et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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