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Current Oncology
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  • Open Access

1 December 2024

Potential Benefits from Physical Exercise in Advanced Cancer Patients Undergoing Systemic Therapy? A Narrative Review of the Randomized Clinical Trials

Freelance Surgeon Oncologist, Residenza Querce, Milanodue, 20054 Segrate, Italy
Curr. Oncol.2024, 31(12), 7631-7646;https://doi.org/10.3390/curroncol31120563
This article belongs to the Special Issue Diet and Physical Activity Management during Cancer
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Abstract

Design. The purpose of this review is the analysis of the literature concerning the effects of physical exercise in cancer patients undergoing medical oncologic treatment. Papers were retrieved from the scrutiny of 15 reviews/meta-analyses published in the last 2 years, which, however, pooled different populations of patients (surgical and medical patients, receiving or not an oncologic therapy, harboring a cancer, or being survivors). Results. We reviewed the data of 35 RCTs on the use of physical exercise in cancer patients, distinguishing well-nourished from malnourished patients. The conclusions of our study are the following: No major difference between well-nourished and malnourished patients as regards compliance/adherence with physical exercise and outcomes. Compliance with physical exercise was reported in about 70% of the studies. Compared with a control group receiving the usual care, in patients who practiced physical exercise, a benefit in some parameters of physical function and quality of life and lean body mass (LBM) was reported in 61%, 47%, and 12%, respectively, of the studies in non-malnourished patients, and in 50%, 100%, and 36%, respectively, of the studies in malnourished patients. The benefit in LBM was more frequently reported in weight-losing patients. There was no strict association among the results of different outcomes (muscle function vs. quality of life vs. LBM). There are still some ill-defined issues, including the optimal physical regimen (with some authors favoring high-intensity interval training and resistance) and the place of exercising (patients usually preferring home exercises, which, however, have been proved less efficacious).

1. Introduction

Depletion of the muscle mass is prevalent in patients with cancer and is more frequent when cancer is in the upper GI tract, pancreas, lung, head and neck, and in the advanced stages of disease [1,2,3,4,5]. Low muscle mass has been consistently associated with adverse clinical outcomes, such as higher morbidity and mortality, dose-limiting toxicity, poor compliance with oncologic therapy, and length of hospitalization [6,7]. Quality of life (QoL) is also affected following cancer diagnosis and is positively associated with muscle mass [8,9,10,11,12,13].
Physical exercise is a globally recognized way of increasing muscle mass in healthy people as well as in elderly sarcopenic ones; however, its potential role in hypoanabolic procatabolic cancer patients is still poorly appreciated in the scientific oncologic community. The current question is whether physical activity is able to support muscle mass and muscle function in advanced cancer patients undergoing an oncologic therapy and whether this might translate into a clinical benefit.
Although several reviews [14,15,16,17,18,19,20,21,22,23,24,25,26,27,28] dealing with the effects of the physical exercise in patients with advanced cancer have been published in the years 2022–2023, it is still difficult to reach an unambiguous conclusion for a variety of reasons. Some reviews simply pool in their analysis the RCTs, unpublished controlled trials, prospective or retrospective comparative studies, or single-arm studies, most include both tumor-bearing patients and survivors, patients undergoing surgery and receiving an oncologic therapy, patients receiving chemotherapy for an advanced tumor and those receiving adjuvant therapy, hence potentially including tumor-free patients. Finally, most of the studies focused on the feasibility of the physical activity as a primary endpoint of the research, and one systematic review and meta-analysis [26] only focused on adverse events, health-care utilization, and treatment tolerability.
The aim of this review is the analysis of RCTs comparing physical exercise versus usual care in patients with an advanced cancer receiving chemotherapy, with a special focus on change in the fat-free mass (FFM) or in the muscle function and their potential correlation with QoL.

2. Methods

The above-mentioned recent reviews [14,15,16,17,18,19,20,21,22,23,24,25,26,27,28] were used to retrieve the pertinent selected literature. In addition, a search of the recent papers published in the first 4 months of 2024 was performed through PUBMED. The inclusion criteria were the same for both the papers retrieved from previous recent reviews and the papers published in the early months of 2024.
We only considered full papers of RCTs in adult cancer patients with an advanced disease, receiving chemotherapy, where the experimental arm underwent a planned program of physical exercises, and the control group was kept under its usual practice. The papers dealing with surgical patients undergoing a preoperative prehabilitation or receiving adjuvant chemotherapy after a successful curative surgery (who can virtually be considered tumor-free) or practicing an exclusive selective physical therapy aimed to potentiate the ventilatory function or the pelvic muscle function in lung cancer or urogenital tumor patients were not considered. Both abstracts and papers not published in English were excluded. Finally, the papers were divided into two large series depending on the baseline nutritional status. Patients were considered malnourished if they had lost weight, or the BMI was below 19.5, or NRS2002 was >3, or the ECOG score was ≥3, or they were receiving tube feeding. The comparison of the effects of physical exercise was always inter-group (and not intra-group), hence the symbol “↑” does not necessarily mean an absolute benefit but also a lower deterioration inthe experimental group as compared with the control group.

3. Results

We collected 35 RCTs (1874 patients) [29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65] and divided them into two groups, one dealing with non-malnourished patients (25 RCTs, 1266 patients) (Table 1 and Table 2), and the other with malnourished patients (10 RCTs, 608 patients) (Table 1 and Table 2).
Table 1. (a) Details of the RCTs in non-malnourished cancer patients. (b) Details of the RCTs in malnourished cancer patients.
Table 2. (a) Results of the RCTs in non-malnourished cancer patients. (b) Results of the RCTS in malnourished cancer patients.
On average, exercise programs had a mean of 3.5 sessions per week, each aerobic session usually included 10–15 min of warm-up, followed by 30 min of training with a wide range of heart rate goals, while in contrast, resistance training often required 10–20 min. Aerobic training aimed at improving VO2 max (or its surrogates), while the goal of resistance training was to increase the muscle mass. Common resistance training included resistance bands and free weights, where participants could perform sets of repetitions in one or more muscle groups with the goal of achieving a pre-specified rating of perceived exertion [30], as described by Borg et al. [66].
Most experiences were in non-malnourished cancer patients and the data of 25 RCTs are reported in Table 1 and Table 2. Lung and GI accounted for the most prevalent primary cancers and median and mean compliance with the planned program of physical exercise were 70% and 70% (r. 37–100), respectively. Most primary endpoints referred to muscle function/physical performance or QoL parameters but at least eight focused on feasibility [35,38,45,46,48,49,51,53]. Median and mean age of patients were 63 and 57.6 (r. 32–66) years, respectively. Patients performed physical exercises for a median period of 3 months, mean 9.3 (r. 2.2–24) weeks. Out of 25 studies, 18 reported the effect of the physical exercises on muscle function and 11 (61.1%) [29,31,32,33,35,42,45,46,47,52,58] showed some benefit, and in 4 of them (36.3%) [31,32,33,52,60] patients also improved their QoL. However, QoL improved also in two studies [30,43] despite no benefit of muscle function. Globally, QoL was evaluated in 19 studies and some items of QoL improved in 9 of them (47.3%). Lean body mass (LBM) change was reported in eight studies and only in one (12.5%) [65] was improved. Finally, four studies evaluated both LBM and QoL: there were no benefits in LBM but only one benefit [65] in QoL.
Ten studies included malnourished patients (Table 1 and Table 2) and the vast majority were patients with GI tumors, especially pancreatic. Four of them focused on feasibility [40,41,56,61] and median and mean compliance were reported in 69% and 68% (r. 59–90) of patients, respectively. The median and mean age of the patients were 61 and 63.2 (r. 57–78) years. Patients performed physical exercises for a median and mean period of 10 weeks and 13 weeks (r. 4–24), respectively. Six studies evaluated the muscle function, and a benefit was observed in three (50%) [44,50,63] and all these three (100%) reported an improvement of QoL. QoL was improved in three [37,57,61] out eight studies (37.5%) and, similarly, LBM changes were reported in eight studies and improved in three (37.5%) [44,50,63] concurrently with a benefit in muscle function. It is noteworthy, however, QoL improved also in one study [37] which did not exhibit any benefit in muscle function.
We attempted to explore whether the number of weeks of exercise and dietary supplementation were related with some outcomes and the findings are reported in Table 3 and Table 4.
Table 3. Outcomes by weeks of exercise.
Table 4. Dietary supplementation and outcomes.
However, we were not able to find any data indicating that the duration of the exercise as well as administration of a nutritional supplementation could affect the results. Especially as regards the duration of the exercise, both positive and negative results were achieved in quite similar time frames. The different methodology of exercise and the impact of different regimens of chemotherapy can account for the difficulty of assessing the more advantageous approach.

4. Discussion

The aim of this review was to define the potential of physical exercise in advanced cancer patients on chemotherapy and mainly relies on the RCTs quoted in the systematic reviews and meta-analyses published in the last two years. Although several scientific societies [66,67,68,69,70] recommend engaging in at least 90 min of moderate-intensity aerobic physical activity per week, in addition to muscle strengthening activities twice weekly, exercise is only performed regularly by a minority of patients diagnosed with cancer [71,72].The conclusion of a recent Cochrane review [73] including only four studies, stating that it was not known if exercise is helpful or safe for people with cancer who experience loss of appetite and weight loss, may have argued, among the oncologists, against a wider use of physical activity.
Our analysis shows that compliance with the physical exercise was about 68–70%, even if estimates of physical activity based on self-report are generally higher than estimates derived from objective measures [74,75,76] and, hence, self-reported adherence must be interpreted with caution. Our findings agree with other meta-analyses [77,78] that show a low incidence of adverse events from participation in exercise oncology clinical trials during treatment and that engaging in exercise during treatment through aerobic exercise interventions and strength training is usually well tolerated without adverse events.
Since we hypothesized that feasibility, compliance, and possibly some outcomes might be different in patients malnourished or not, we separately examined these two series of studies. However, data show that adherence to the program of physical exercise was almost identical, 70% versus 68–69% in non-malnourished and malnourished patients, respectively. There was some benefit as regards the muscle function in 61% versus 50%, the QoL in 47.3% versus 100%, and LBM in 12.5% versus 37.5% of studies on non-malnourished and malnourished patients, respectively. The better response of the physical exercise on LBM in malnourished patients might be due to the combination of the physical exercises with a supervised nutritional support in six of ten of these studies, might simply reflect a major hindrance in increasing LBM in subjects who do not have a baseline muscle mass depletion.
Due to the impossibility of considering all variables (type of tumor, oncologic treatment and response, duration, and characteristics of the exercise regimen etc.) affecting the response to the exercise in the different studies, a formal statistical analysis was not performed; however, it appears that the duration and combination with a nutritional supplement did not affect the outcome (Table 3 and Table 4).
The most intriguing observation was the frequent dissociation of the response of the different endpoints. For instance, in one study [50], muscle function and LMB improved but QoL did not, and on the contrary, QoL improved in a study [37] without any positive response of the muscle function. However, in three studies [44,50,63] where LBM improved, there was a concurrent benefit in muscle function. Overall, these data should warn the clinicians to not consider muscle function and LBM as a surrogate of QoL.
The analysis of the literature shows that there are two major issues which remain unresolved, and these certainly represent a limitation of our analysis.
The first concerns the option of home versus supervised exercise. Comparing with home exercise programs, supervised sessions appear to generate higher adherence and social support and improve both role and emotional functioning [79], likely through interactions with supervising personnel and peers in the exercise setting. This would also provide a number of additional benefits to participants with a poor prognosis and symptomatology [80,81]. Kuehr et al. [82] showed a 95% adherence rate in a hospital-based exercise program and 77% adherence rate in a home-based program, while Quist et al. [83] reported a rate of 73.3% and 8.7% in supervised group training and home-based training, respectively. Consequently, supervised exercise programs (especially resistance training) appear more effective than non-supervised ones [44,61,84]. Notably, most patients prefer home-based exercises [85], even if accessibility of the location would appear to be more important than the type of location [51,86]. Since at-home exercise programs may be related to self-efficacy at baseline, they might be a better option for patients with high self-efficacy and motivation [87]. To improve the adherence to the exercises the use of step trackers or of accelerometers or recalls by phone have been proposed [88].
The second issue which warrants further deep exploration in future studies is the modality of the exercises. Most of the RCTs reported in this review, as well as the guidelines by American College of Sports Medicine, propose a combination of both resistance and endurance training in cancer patients, since concurrent training can induce wide-ranging physical adaptations promoting both aerobic (VO2 max and resistance to fatigue) and anaerobic (muscle strength and function) components simultaneously, without any adverse effect in cancer patients. This is in keeping with both the guidelines of the American College of Sports Medicine as well as with other studies not considered in this report [89,90,91,92]. However, some patients with advanced gastrointestinal cancer [93] would prefer resistance exercise training since resistance exercise training has a higher potential for individualization. While general recommendations include primarily aerobic exercise of moderate intensity, the definitive superiority of one exercise modality over another is still uncertain, especially in advanced-stage lung cancer patients [67]. This review shows that several regimens of physical exercise were applied in the different studies because the optimal training program is still ill-defined. Reljic et al., [53] following the observation that the fatigue was a common reason for the participant reporting difficulty performing their prehabilitation schedule, favored the incorporation of low-high-intensity interval training into exercise programs and/or to implement it as an initial preparatory training modality before higher-volume exercise regimes. Toohey et al. [94] showed that low-volume high-intensity training was associated with greater improvements in cardio-respiratory fitness, lower body strength and waist circumference compared with traditional continuous low- to moderate-intensity exercise training, even if in a previous study, the same authors [95] reported that the low-volume high-intensity program was well tolerated by the participants and hence was probably the preferred modality to improve fitness. Three recent systematic reviews and meta-analyses [95,96,97] reported that high-intensity interval training was superior compared to usual care in improving physical fitness, peak oxygen consumption, and health-related outcomes across all stages of therapy and aftercare. Currently, there is no evidence for the benefits of high-intensity interval training compared to aerobic training of moderate intensity for changes in cardiorespiratory fitness, LBM, and patient-reported outcomes [21]. Recent studies [98,99,100] have shown no significant differences between high-intensity interval training and control groups in terms of body composition, but high-intensity interval training prevented body weight increase in breast cancer patients compared to the usual care control group. More recently, the use of whole-body electro-myostimulation has been proposed as a way of potentiating the biomechanical function of muscle [101].
Further limitations of this paper concern the heterogeneity of patients included in different RCTs as well as in the same study, which precludes a more precise analysis by type of primary.
However, there are some points of force, as follows: a good compliance and adherence to the physical exercise program was commonly reported, some primary endpoints were achieved (muscle function and QoL in half or more of the studies and LBM in a lower rate), and the presence of malnutrition was not a major hindrance to the programs as regards both the compliance/adherence and the outcomes. Additional randomized and controlled studies are needed to determine the optimal intensity and quantity of training programs to achieve possible positive effects. More important, patients and their formal and informal caregivers should be alerted that exercise is safe and feasible, can be tailored to individual needs and levels of functioning, and can be performed both at home without supervision and in a supervised setting. Finally, an important topic which was beyond the scope of this review but is of utmost importance, is the possibility to achieve, through the physical exercise, a better response to the oncologic treatment as recently shown by randomized [102] and non-randomized studies [65].

Funding

This research received no external funding.

Acknowledgments

I am grateful to BF for the invaluable help in retrieving the literature and ordering it in the tables.

Conflicts of Interest

No conflicts of interest; no funding supported this study.

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