Promoting physical activity among cancer survivors: an umbrella review of systematic reviews

Purpose Exercise is the core element of rehabilitation for cancer patients. However, most of the patients’ exercise levels failed to meet the indicators recommended by the guidelines or even decreased. Therefore, this umbrella review aims to provide an overview of review articles addressing the evidence of interventions to promote physical activity behavior change and increase physical activity among cancer patients. Methods We searched nine databases from inception to 12 May 2022 to obtain systematic reviews and meta-analyses of interventions to promote physical activity among cancer patients. The AMSTAR-2 was used for the quality assessment. Results Twenty-six individual systematic reviews including 13 studies performed meta-analyses. A total of 16 studies’ designs were all in randomized controlled trial. Most reviews included studies that were mainly delivered in home settings. The most frequent and mean duration of the interventions was 12 weeks. Interventions mainly included electronic, wearable health technology-based, behavior change techniques (BCTs), and theory-based strategies. Conclusions Electronic, wearable health technology-based, BCTs, and theory-based interventions were effective and feasible in promoting physical activity in cancer survivors. Clinical practitioners should take corresponding intervention measures according to the characteristics of patients in different groups. Implications for cancer survivors Future research may benefit cancer survivors by more comprehensively applying electronic, wearable health technology-based, BCTs, and theory-based interventions. Supplementary Information The online version contains supplementary material available at 10.1007/s00520-023-07760-0.


Background
With socio-economic development and the prevalence of various cancer risk factors, the burden of cancer morbidity and mortality worldwide is increasing rapidly [1,2]. In 2020, there are an estimated 1930 million new cancer cases and nearly 10 million cancer deaths worldwide [1]. Cancer patients have a higher cure rate and survival rate under the popularization of early screening and the progress of medical technology. Exercise is one of the vital measures for rehabilitation of many chronic diseases, improving the quality of life and reducing mortality [3,4]. At the same time, exercise has a positive impact on anxiety, depression, fatigue, and quality of life decline caused by cancer or treatment [5]. Therefore, multidisciplinary cancer teams should encourage cancer patients to exercise.
Aerobic exercise and resistance exercise are safe, feasible, and effective in cancer patients during and after adjuvant therapy [6,7]. According to the exercise guide for cancer patients, cancer patients should gradually resume their daily activities after surgery and recommended at least 150 min of aerobic exercise and 2 ~ 3 times of resistance training per week [5]. However, few patients can achieve this index. A 1-year study by Arem et al. [8] found that only 33% of women reached 150 min of exercise per week, suggesting that the physical activity (PA) level of breast cancer patients during treatment was reduced, and they also had less activity Qiu, Lin and Ye, Maodie contributed equally to this work and should be considered co-first authors.

Inclusion/exclusion criteria for study selection
The inclusion criteria for this umbrella review according to PICOS format are as follows: (1) types of participants, cancer patients either completed or undergoing treatment; (2) types of interventions, any interventions that may promote or maintain physical activity behavior change and adherence, including but not limited to the motivational strategies, eHealth interventions, and behavior change techniques; (3) types of comparison, compares the intervention to an alternative intervention or usual care; (4) types of outcome, the primary outcome was physical activity behavior (self-reported or objectively measured) and secondary outcomes were including but not limited to physical activity adherence, self-efficacy, physical function, and quality of life; (5) types of studies, systematic reviews and meta-analyses of a quantitative or qualitative study. Criterion (5), systematic reviews that include qualitative and quantitative studies, aims to enrich the evidence.
Studies were excluded if they (1) reported the efficacy of a physical activity intervention that did not involve physical activity level or adherence or (2) were available as a conference abstract only.

Selection of studies and data extraction
Importing all search results into EndNote X9, title and abstract screening were conducted concurrently by two investigators trained in evidence-based courses (e.g., training in theories, principles, and methods of evidence-based medicine). If the title and abstract lack sufficient information to make a decision, the article was carried forward to the full-text screening stage. Full texts were obtained and screened independently by two investigators according to the inclusion and exclusion criteria of the literature.
The included literature was extracted after the literature quality evaluation by the self-designed standardized table to extract data; the main extracted content are as follows: title, first author, publication year, objective, study designs, number of studies included, analysis method, quality assessment tools, population, intervention, outcome measure, etc. Two researchers did data extraction independently, and inconsistencies were resolved by discussion.

Methodological quality assessment
The methodological quality of the included systematic reviews and meta-analyses was assessed using AMSTAR-2 [12], which includes 16 items. According to the instrument, two reviewers classified the results of included systematic reviews as high, moderate, low, and critically low. If the study has no or one non-critical weakness, we appraised it as high; if more than one noncritical weakness, we appraised it as moderate; if one critical flaw with or without non-critical weakness, we appraised it as low; and if more than one critical flaw with or without non-critical weakness, we appraised it as critically low.
Our study was founded on the concept of evidence from multiple sources. Included studies had interventional and qualitative studies. At the same time, the interventions and outcome indicators of this study are diverse, and the Grading of Recommendations Assessment, Development and Evaluation (GRADE) is not applicable. Therefore, the evidence was pre-ranking using the Joanna Briggs Institute evidence pre-ranking system [13]. According to the type of included studies, it is divided into five levels from level 1 to 5.

Data analysis
Due to the factors such as different intervention techniques, different application times, and different research objects, this study only conducts a descriptive analysis of the included studies.

Literature selection
The initial search resulted in 1129 records through database searching; after the removal of duplicates, 820 records remained. Of these, excluded after title, abstract, and fulltext screening according to the selection criteria, resulting in 26 articles. (Fig. 1).

Methodological quality and evidence grade evaluation
The methodological quality evaluation results showed that 1 study was high, 10 were intermediate, 9 were low, and 6 were very low. Among the 7 key items of AMSTAR 2 quality evaluation, item 2 and item 15 have significant defects; the non-critical items with obvious defects are item 3 and item 10 (details in Figure S1). The results of the level of evidence evaluation showed that 16 articles were ranked as 1a, that is, systematic reviews of multiple RCTs; 10 articles were ranked as 1b, that is, systematic reviews of multiple RCTs and other interventional studies.

Intervention settings
Intervention settings in our reviews included studies that included group, one on one, home, clinic or research-setting, and center-based. Most reviews included studies that were mainly delivered in home settings [9, 15, 19, 20, 23-25, 27-29, 38]. Some reviews that delivered in a variety of settings included a combination of supervised and home-based exercise, supervised combined with unsupervised [14,16,19,26,30]. In reviews that focused on a single intervention setting, all were conducted in a home setting [18,33]. Home-based exercise usually has behavioral support, including information feedback, ongoing interaction, or counseling with the research team. Five reviews did not report the setting [17,32,34,36,37]. Interventions that included a home-based training component seemed more effective than clinics or gyms in a meta-analysis of 27 studies (β = 0.261; 95% CI = 0.135, 0.386; P ≤ 0.001) [23]. And the review by Rossi et al. [25] indicated that home-based combined center-based interventions may increase physical activity more than home-based programs alone among overweight and obese female cancer survivors.

Intervention length
The intervention length varied from 2 weeks to 4.78 years. The most frequent and mean duration of the interventions was 12 weeks [14,18,20,29,30,32,34]. Four reviews included the length of reporting ranging from a minimum of 12 weeks [16,19,25,33], four reviews included the length of interventions ranging to 12 months [23,24,35,36]. The studies included a one-time recommendation, or follow-up during intervention and post-intervention, as Grimmett et al. [27] included a physical activity behavior follow-up assessment ranging from 3 months post-intervention to 5 years post-intervention. The review by Singh et al. [36] indicated that interventions lasting 12 weeks (SMD = 0.73) were greater at increasing MVPA compared with interventions < 12 weeks (SMD = 0.19; x 2 = 4.78, p = 0.03). And interventions are effective for a moderate increase in physical activity at least 3 months after the intervention (interventions detail in Table S1) [27].

Electronic interventions
Investigating the effect of electronic interventions on cancer survivors were 34.61% (n = 9) of the total included studies [17,18,22,24,28,31,32,34,36,38]. Of these, seven studies aimed at the effect of electronic health (eHealth) on exercise levels in cancer patients [17, 22, 24, 31, 32, 34, The length of interventions ranged from 4 weeks to 6 months. DBCIs may improve PA and BMI among cancer survivors. Self-monitoring of behavior, goal setting (behavior), credible source and feedback on behavior were the most frequently described BCTs Mean intervention length was 10 months. The transtheoretical model (n = 3), social cognitive theory (n = 3), and theory of planned behavior (n = 2) were the most used theories. "goal setting (behavior)" (n = 10), "goal setting (outcome)" (n = 10), "action planning" (n = 9), and "problem solving" (n = 9) were the most commonly used BCTs. Intervention modalities were primarily print material based (n = 4) and telephone counseling (n = 4). Theory-based PA interventions for colorectal cancer survivors are effective in improving PA uptake among CRC survivors 1a    [14] Eight out of the ten identified studies reported positive intervention effects on aerobic physical activity behavior The most frequent duration of the interventions was 12 weeks. The most commonly employed behavior change techniques were self-monitoring and goal-setting, eliciting social support and positive reinforcement. 12-week interventions employing behavior change techniques derived from a variety of theories and delivered in a variety of settings (i.e., one-on-one, group or home) can be effective at changing the aerobic physical activity behavior of breast cancer survivors in the mid-to long terms Brunet et al. 2020 [30] • Two studies reported within person increases in physical activity behavior and one reported decrease • Nine studies reported between-group differences in physical activity behavior favoring the intervention group Mean intervention length was 15 weeks, and the most frequent duration of the interventions was 12 weeks. Seven of these used the social cognitive theory, one used the theory of planned behavior, and one used selfmanagement principles. Two studies used motivational interviewing and narrative therapy. The most commonly used BCTs were "goal settingbehaviors" (n = 7), ":self monitoring of behavior" (n = 5), and "problemsolving" (n = 4) Health care provider-delivered physical activity interventions may help to increase cancer survivors' physical activity behavior 1a Dorri et al. 2020 [17] The majority of studies (10/16) reported positive effects on PA (p < 0.05) The technology used in included studies comprised web based, mobile-based (apps), web-and-mobile-based apps as well as email. The mobile apps used were Lose it!, Smart After Care, GAINFitness, MapMyFitness, and Fitbit The use of eHealth tools is effective in promoting PA in BC patients and can be used as a supportive opportunity for these patients 1b Most studies were a 12-week trial. The Fitbit One, Polar A360/M400, activ-PAL, and Garmin Vivofit smartwatches were most popular as an intervention component. increased moderate-to-vigorous intensity physical activity was observed to be associated with increased perceived cognition and higher cognitive performance. Wearable health technology-based physical activity interventions to be effective for improving physical activity, attitude, and cognitive functions and for reducing sedentary behavior, anxiety, and worry in BCS 1b Cheung et al. 2021 [38] All studies(8) investigated interventions for pediatric cancer survivors to increase their physical activity level The intervention period lasted between 6 weeks and 6 months. eHealth and mHealth interventions showed effectiveness and feasibility to promote physical activity among pediatric cancer survivors 1a Ester et al. 2021 [32] Significant post-intervention PA increases were noted in 52% (35/67) of the studies Across studies with a median of 12 weeks. Social cognitive theory (23/67, 34%) was the most used theory. The mean number of BCTs used across the studies was 13.5 (SD 5.5), with self-monitoring, credible sources, and goal setting being used in > 90% of studies. Weight analyses showed the greatest associations between increased PA levels and PA as a primary outcome, interventions using websites or mobile apps, interventions integrating multiple behavioral theories, and interventions using BCTs of problem solving and action planning A range of eHealth PA interventions may increase PA levels among adults affected by cancer, and specific components (e.g., websites, use of theory, and action planning) may be linked to greater effectiveness 1b Khoo et al. 2021 [34] • Seven (7/8) reported significant effects of mHealth interventions with personal contact on MVPA • Six non-controlled trials reported on MVPA, of which two reported a significant effect favoring the mHealth intervention • Four studies (4/31) reported a significant decrease in SB following an mHealth intervention Researchers that assessed an mHealth intervention and its effects on MVPA in controlled studies were often 12 weeks long. Activity trackers being the most commonly used mHealth technology. There is strong evidence for mHealth interventions, including personal contact components, in increasing moderate-to-vigorous intensity PA among cancer survivors. However, there is inconclusive evidence to support mHealth interventions in increasing total activity and step counts 1b 38]. eHealth uses technologies including telephones, websites, email, and mobile health (mHealth) technologies. The majority of studies (6/7) [17,22,24,32,34,38] reported that eHealth interventions were effective and feasible in promoting physical activity in cancer survivors. eHealth resulted in a significant increase in MVPA minutes/week (MD = 41; 95% CI = 12, 71; p = 0.006) in a meta-analysis that included 5 RCTs and 2 pre-post studies [22]. Compared with the control interventions, eHealth technology provides communication (including real-time, automated reminders) and feedback. Three studies were included which aim to examine the feasibility of digital activity trackers in cancer survivors and their effects on activity levels. And activity trackers were the most commonly used mHealth technology [34], and interventions based on physical activity trackers and pedometers usually include BCTs or theory-based interventions [22,36]. In the included studies, wearable physical activity trackers mainly include Fitbit One, Polar A360/M400, GT3X + Acti-Graph, ActivPAL, and Garmin Vivofit smartwatches. Four reviews [18,28,31,34] found that wearable health technology-based physical activity interventions are effective in improving physical activity, and health-related outcomes in individuals with cancer. The review by Khoo et al. [34] indicated there is strong evidence that mHealth includes an individual exposure component to increase moderate intensity PA in cancer survivors. And physical activity tracker and pedometer-based interventions had moderate-to-large effects (all p < 0.05) on the duration of moderate-intensity physical activity (SMD = 0.87; 95% CI = 0.43, 1.32), MVPA (SMD = 0.61;95% CI = 0.36,0.86), total physical activity (SMD = 0.62; 95% CI = 0.39, 0.84), and daily steps (SMD = 0.54; 95% CI = 0.30, 0.78) in a meta-analysis of 15, 16, and 19 studies, respectively [36]. Subgroup analysis by Singh et al. [36] showed that baseline counseling (compared to no baseline counseling taken) and theory-based were effective in increasing PA levels, respectively.

Behavior change techniques and theory-based interventions
Among the included studies, five studies were limited to behavioral change techniques (BCTs) and theory-based interventions [9,19,20,23,25], and five studies related to integrated interventions [14,26,30,35,37]. BCTs in the included studies were seven [9,14,23,26,30,35,37]. BCTs had a significant effect on PA levels in a meta-analysis of 30 studies (g = 0.28; 95% CI = 0.18, 0.37; I 2 = 54.29%) [23]. Motivational strategies improved MVPA duration in a meta-analysis of 10 studies (SMD = 0.55; 95% CI = 0.30, 0.79; I 2 = 51.4%) [20]. The most commonly used BCTs were goal setting (behavior), goal setting (outcome), action planning, habit reversal, instruction on how to perform the  [9] Potential of the intervention to increase PA behavior; "very promising" (n = 11), "quite promising" (n = 13) Interventions lasted from 8 to 104 weeks. Demonstration on how to perform the behavior was the most commonly used BCT (n = 23). Adding objects to the environment (pedometer or accelerometer) was the BCT with the highest potential to increase PA. This was followed by goal setting and self-monitoring of behavior. "Instructions on how to perform the behavior," "goal setting," "self-monitoring," and adding a pedometer or accelerometer into the environment in combination appear to have a beneficial effect on PA. behavior, self-monitoring, eliciting social support, positive reinforcement, and problem-solving. And effect sizes did not increase meaningfully with the number of BCTs per intervention (β = 0.005; 95% CI = − 0.007, 0.017; P = 0.408) [23]. The BCTs prompts, reduce prompts, graded tasks, non-specific rewards, and social rewards were significantly associated with larger effects, while information about emotional consequences and social comparison was associated with smaller effects size [23]. Face-to-face behavior change counseling interventions improved physical activity behavior in a meta-analysis of 13 studies (SMD = 0.22; 95% CI = 0.11,0.33; p < 0.001; I 2 = 6%) [35]. Supervision is most important for adherence [26], and involved supervised exercise sessions were associated with greater effectiveness in a meta-regression of 54 studies (B = 0.20, SE = 0.07, p = 0.005) [29]. Four reviews involved theory-based behavioral interventions [19,25,30,37]. Most studies cited the social cognitive theory, the transtheoretical model, and the theory of planned behavior. Most reviews suggest that theory-based PA interventions can increase PA in cancer survivors. Theory-based PA interventions among colorectal cancer survivors improve physical activity in a meta-analysis of 8 studies (ES = 0.26; 95% CI = 0.13, 0.38; I 2 = 16%) [37]. Behavior change theories had medium improvements in self-reported physical activity in a meta-analysis of 12 studies (SMD = 0.57; 95% CI = 0.33, 0.80; I 2 = 67%) [19]. And there were smaller effect sizes for TPB-based interventions in a meta-analysis of 7 studies [23]. The included review based on 16 studies [20] showed that the combination of step trackers with counseling, printed materials, or motivational strategies based on behavioral change theory provided a consistently positive effect on adherence to self-directed PA among breast cancer survivors.

Psychoeducation
Dennett et al. [21] evaluated the effectiveness of psychoeducational interventions in physical activity behavior change among cancer survivors. This review of 2 randomized controlled trials demonstrated that adding psychoeducation to exercise rehabilitation programs had no additional benefit in improving physical activity behaviors or improving health outcomes in cancer survivors.

Other interventions
Five studies were included to assess the effectiveness of interventions in promoting physical activity [15,16,27,29,38]; interventions in included studies were workshops, group exercise, walking, behavioral counseling, home-based/ group-supervised exercise classes, counseling, and group discussions, printed materials and pedometer, etc. Most studies use a combination of interventions for exercise promotion intervention. Reviews indicate that both group and individual PA interventions for individuals have had positive outcomes. Too frequent direct supervision may not be better for physical activity levels. And greater contact time was associated with increased effectiveness in a meta-regression of 63 studies (B = 0.002, SE = 0.001, p = 0.008) [29]. Reasonably low-intensity interventions may be sufficient to induce lasting behavioral change in positive, young, well-educated, and white populations, but other populations may require more intensive support, especially older and physically constrained populations. Overweight or sedentary participants had larger effect sizes on PA levels in a meta-regression of 84 studies (B = 0.15, SE = 0.07, p = 0.03).

Adverse events
Seven of the included reviews [21, 24-26, 33, 36, 38] reported the adverse reactions of patients during exercise intervention (26.9%, n = 26), and 19 reviews [9, 14-20, 22, 23, 27-32, 34, 35, 37] did not report and mention on adverse events at all. The review of Cheung et al. [38] showed that no major adverse events occurred in the 8 studies involving pediatric cancer survivors. And the study by Haberlin et al. [24] including 10 studies involving eHealth used interventions showed that no adverse effects have been reported. Adverse events included minor joint injuries/soreness [25,36], recurrence of previous tendinitis [33], plantar fasciitis [26,36], and falls [36]. In the exercise intervention of overweight and obese women, there is a serious adverse event, a pelvic stress fracture, was reported [25].

Discussion
Exercise is one of the vital rehabilitation strategies for cancer patients. This umbrella review summarized evidence from systematic reviews and meta-analyses on interventions that improve exercise levels and maintain or improve exercise compliance in cancer patients. The main findings of our umbrella review were that (1) the most frequent and mean duration of the exercise interventions was 12 weeks, and 3 months post-intervention completion can be assessed and guided; (2) electronic, wearable health technology-based, BCTs, and theory-based interventions were effective and feasible in promoting physical activity in cancer survivors; promoting exercise requires a combination of interventions; (3) digital activity trackers were the BCTs with the highest potential to increase PA; (4) the BCTs prompts, reduce prompts, graded tasks, non-specific reward, and social reward were significantly associated with larger effects, while information about emotional consequences and social comparison were associated with smaller effects size; and (5) higher BMI was associated with higher intervention effects, and interventions targeting overweight or sedentary participants were particularly effective.
In this umbrella review, most of the interventions reported statistically significant results for PA outcome in cancer patients. Studies [17,22,24,32,34,38] have shown that electronic interventions are expected to improve the level of exercise in cancer patients. Particularly, physical activity tracker and pedometer-based interventions had moderate-to-large effects on duration of moderate-intensity physical activity [36]. eHealth is used as an auxiliary tool for exercise intervention. Most studies [22,34,36] on eHealth usually include counseling, educational sessions, personal contact, and BCTs. And baseline counseling is necessary for cancer patients during exercise intervention [35,36]. There is strong evidence for BCTs in increasing moderate-to-vigorous intensity PA among cancer patients. It is worth noting that not all technologies seem to be applicable, and the effect of intervention may not increase with the increase of the number of BCTs per intervention. BCTs combining with activity trackers is the highest potential to increase PA [23]. Most of the studies show the importance of interaction and behavioral intervention on the exercise behavior of cancer patients, and there are few studies considering the maintenance of exercise behavior after intervention [16,18,24,27,32]. At the same time, the importance of personal contact components was also found in this umbrella review, but the frequency of assessment or feedback in exercise intervention needs further study.
Although exercise has been advocated, cancer survivors face a series of factors that may impede or facilitate their participation in physical activity. The key barriers to exercise were treatment-related side effects, lack of time, and fatigue [39]. And the critical facilitators of exercise include improved physical health, improved mental well-being, gaining control, and the social benefits of exercise [39]. And fatigue is one of the most commonly reported side effects of cancer treatment [40,41]. About 70% of cancer patients receiving chemotherapy or radiotherapy have cancer-related fatigue [41]. Many studies have shown that exercise can effectively alleviate the fatigue of patients while improving other adverse reactions, as well as improving physical function and quality of life [42,43]. However, fatigue is also one of the main obstacle factors for patients' exercise. Therefore, it is particularly important to improve the exercise level of patients through intervention measures. The study by Machado et al. [44] showed that exercise training is an effective intervention to reduce CRF, especially in patients receiving chemotherapy. Similar to previous studies [45][46][47], by guiding patients in time management; providing effective, time-saving, and personalized exercise programs; and supporting relevant electronic equipment and network platforms, patients can be promoted to exercise. However, most of the participants in the included systematic review were in the post treatment, and more evidence is needed for measures related to PA level improvement in cancer patients undergoing treatment.
To our best knowledge, this umbrella review is the first to summarize the interventions for promoting physical activity. In similar studies on different populations, most of the physical activity promotion studies focus on children; few studies focus on adolescents or the elderly [48,49]. In our study, most interventions tend to be a combination of approaches, including electronic, wearable health technology-based, BCTs, theory-based, and combined interventions. Disease treatment seeks targeted intervention, and if exercise intervention can be targeted, it can also maximize the patient's exercise level and exercise compliance. The study by Rossi et al. [25] found that among overweight and obese female cancer survivors, homebased integration of center-based physical activity interventions may improve patient activity levels more than homebased programs alone. Interventions are more effective in overweight or sedentary patients than in overweight and obese women. Supervision of sedentary patients is the most important measure to improve compliance [26]. However, in terms of interventions for different symptoms, more research is needed to explore the better effectiveness of different interventions.

Limitation
The quality of the comprehensive review depends on the quality of the included reviews, which in turn depends on the quality of the primary study. Therefore, we need to consider the limitations of the study. First, moderate to high-grade studies were limited as assessed by the AMSTAR 2, mainly related to the study's protocol design and reporting, and investigation and discussion of publication bias, a common mistake in most systematic reviews. Second, although the incidence of adverse events was low in the reported studies, the included reviews lacked monitoring of the adverse effects of exercise interventions. Finally, the details of the intervention still need further research, including the effect of duration and frequency on patients' physical activity levels.

Conclusion
Oriented to positive health and modifiable factors, our study provides an overview of strategies used in the field of exercise promotion, clarifying the intervention setting, duration of intervention, and intervention strategies. It provides an evidence-based basis and reference for clinical practitioners who need rapid access to evidence related to the promotion of exercise in cancer patients. There is abundant evidence that eHealth, wearable health technology-based (combine with theory, BCTs, counseling, etc.), BCTs, and theory-based interventions were effective and feasible in promoting physical activity in cancer survivors. Faced with different groups of patients, such as overweight, sedentary behavior, the elderly, and limited physical activity, appropriate interventions should be adopted according to the characteristics of the population.