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. 2023 Apr 8;10(7):4274–4285. doi: 10.1002/nop2.1725

The content and effectiveness of physical activity for cancer‐related fatigue among colorectal cancer survivors: Systematic review and meta‐analysis

Liangrong Geng 1, Xiaoyu Li 1, Liqun Guo 1, Rui Zhang 1, Shujin Yue 1,✉
PMCID: PMC10277440  PMID: 37029592

Abstract

Aims

To review the content and efficacy of physical activity (PA) for cancer‐related fatigue (CRF) among colorectal cancer survivors.

Design

Systematic review.

Methods

A comprehensive search for randomized controlled trials from inception to April 1, 2022, of the following database was performed: EMBASE, PubMed, Web of Science, Cochrane Library, China National Knowledge Infrastructure (CNKI), Wanfang Data and China Biology Medicine (CBM). RevMan5.4 software was used for performing meta‐analysis.

Results

A total of eight qualified randomized controlled trials that included 542 survivors were included. PA interventions significantly reduced the CRF (SMD = −0.46; 95% CI: [−0.76, −0.15], Z = 2.67, p = 0.003); Subgroup analysis showed that fatigue was significantly improved when the length of interventions was at least 6 months and the weekly duration of PA was less than 150 min/week (SMD = −0.54; 95% CI: [−0.81, −0.27], Z = 3.87 and p = 0.0001; SMD = −0.67; 95% CI: [−1.15, −0.19], Z = 2.74 and p = 0.006); PA intervention with the length of <6 months and the volume of ≥150 min/week did not reduce fatigue (p > 0.05).

Keywords: colorectal cancer, fatigue, physical activity, survivors

1. INTRODUCTION

Colorectal cancer (CRC) is the third most frequent cancer globally; according to the latest data, the incidence of new colorectal cancer cases was as high as 10%, and the number of new cases worldwide reached 1.93 million in 2020 (Sung et al., 2021). One of the most common treatment options for CRC in clinical practice is radical resection combined with chemotherapy, which has greatly improved the survival rate (Iveson et al., 2019). However, the quality of life of CRC patients has not been promoted significantly due to the many adverse effects caused by cancer itself and treatments, especially chemotherapy, such as chronic pain, sleep disturbances, fatigue, depression and so on (Ketelaers et al., 2022; Sakr et al., 2020). Therefore, the burden of follow‐up care for CRC survivors is expected to increase, and exploring ways to improve cancer‐related symptoms and quality of life in this population deserves attention.

Cancer‐related fatigue (CRF), a sustained and distressing sense of tiredness or exhaustion, is currently recognized as one of the most common and bothersome symptoms that extremely affects the physiology and psychological state, social activities and quality of life among CRC survivors (Rau et al., 2020). CRF has the following characteristics compared with ordinary fatigue among the general population: CRF is caused by cancer or cancer treatments; it includes subjective sense and objective manifestations, while the relationship between them is not a simple correlation, and having subjective feelings does not necessarily have objective manifestations. The subjective sense mainly includes three dimensions: physical fatigue, emotional fatigue and cognitive fatigue, and the objective manifestations mainly show a decrease in physical fitness and energy (Berger et al., 2015). One of the most typical characteristics of CRF is usually peaks immediately, which is experienced by almost all cancer survivors and can be up to 10 years after diagnosis (Gernier et al., 2020). A recent longitudinal study also indicated that 80% of the included oncology patients (n = 1332) undergoing chemotherapy experienced moderate to high levels of fatigue (Morse et al., 2021). However, the negative impact of CRF has not received sufficient attention from the managing staff (Hladschik‐Kermer et al., 2013). Given the poor management and severity of CRF, it is a high priority in growing safe and well‐tolerated supportive interventions to improve the symptom throughout the trajectory of the treatment among CRC patients (Takahashi, 2022).

Currently, due to the pharmacological treatment for CRF is not effective enough and some drugs have serious adverse effects, the preferred treatment for CRF is non‐pharmacological, including physical exercise, psychological intervention and nutritional support (Takahashi, 2022). Based on the current level of favourable clinical outcomes, physical activity (PA) has been considered to be one of the most beneficial interventions in preventing or relieving fatigue and has been recommended in the clinical guidelines (Okely et al., 2021; Thong et al., 2020). Several systematic reviews and meta‐analyses concluded the effects of PA intervention on CRF (Andersen et al., 2022; Liu et al., 2021; Medeiros Torres et al., 2022; Toohey et al., 2022; Van Vulpen et al., 2020), and most of these studies showed positive outcomes (Liu et al., 2021; Medeiros Torres et al., 2022; Toohey et al., 2022; Van Vulpen et al., 2020). However, there is significant heterogeneity due to these studies mainly focusing on survivors diagnosed with breast cancer or prostate cancer (Andersen et al., 2022; Liu et al., 2021; Medeiros Torres et al., 2022; Toohey et al., 2022; Van Vulpen et al., 2020).

Thus far, a total of six meta‐analyses have reviewed the efficacy of PA intervention on CRF in CRC patients (Brandenbarg et al., 2018; Cramer et al., 2014; Dun et al., 2020; Jung et al., 2021; Machado et al., 2022; Singh et al., 2020), however, evidence remains ambiguous, half of them showed PA intervention has no effects on CRF (Brandenbarg et al., 2018; Cramer et al., 2014; Jung et al., 2021), while others found exercise can effectively reduce CRF only in some specific subgroups (Dun et al., 2020; Machado et al., 2022; Singh et al., 2020). For example, Machado et al. found that PA intervention was only effective for patients with CRC who were undergoing chemotherapy and was marginal for those who were post‐treatment through a subgroup analysis of whether patients were during or after treatment (Machado et al., 2022). Another meta‐analysis conducted by Dun et al. indicated that moderate PA intervention can reduce CRF but vigorous PA intervention did not (Dun et al., 2020). Nonetheless, the study developed by Dun et al. included both randomized controlled trials and non‐randomized controlled trials, so the conclusion should be interpreted with caution as it is methodologically erroneous to combine the two different study types for a quantitative meta‐analysis (Dun et al., 2020). Notably, it is known that the efficacy of different contents of exercise for CRF has a large variability (Machado et al., 2022), hence, it is necessary to identify the optimal content of PA interventions. However, subgroup analysis of the different modes, lengths and volumes of PA interventions has not been performed in all reviews mentioned above. Besides, due to the low quantity and high heterogeneity of the included eligible trials, the findings of these systematic reviews were limited by the decreased external validity and the increased possibility of type II error. In addition, only one systematic review excluded the trials if the effect included a nonphysical activity intervention (Machado et al., 2022), which could lead to the lack of power to identify the association between PA and CRF given that the nonphysical activity interventions may also reduce CRF. Overall, it remains challenging for CRC survivors to select optimal modes, lengths or weekly duration of PA interventions for reducing CRF based on current evidence. Therefore, there is a need to include the latest relevant RCTs and perform an updated systematic review considering that only studies up to 2020 and English articles were included in the previous meta‐analyses. This study is hence designed to conduct a subgroup analysis to compare the effect of PA on CRF between different modes and lengths of exercise, gain insight into the content and efficacy of PA interventions and make suggestions for healthcare staff on how to support CRC survivors with CRF.

2. METHODS

2.1. Search strategy and study selection

A systematic literature review designed to build an overview of usable evidence on PA for CRC survivors with CRF was performed. We performed a thorough search of the following database from inception to 01 April 2022, without language restrictions: EMBASE, PubMed, Web of Science, Cochrane Library, China National Knowledge Infrastructure (CNKI), Wanfang Data and China Biology Medicine (CBM). Chinese databases were also included to widen the range of literature search and the combinations of MeSH and free‐text words were used for ‘colorectal cancer’, ‘physical activity’ and ‘fatigue’; they included ‘exercise’, ‘exercise therapy’, ‘exercise training’, ‘aerobic exercise’, ‘physical activity’, ‘lifestyle intervention’, ‘colorectal neoplasm’, ‘colorectal cancer’, ‘colonic neoplasm’, ‘colon cancer’, ‘colon tumour’, ‘rectal neoplasm’, ‘rectal cancer’, ‘rectal tumour’, ‘fatigue’, ‘cancer‐related fatigue’, ‘cancer‐related fatigue’, ‘CRF’, ‘quality of life’, ‘HRQOL’, ‘health‐related quality of life’ and ‘QOL’. In addition, the reference lists of the included studies and the grey literature were searched manually for a supplement.

2.2. Inclusion and exclusion criteria

The inclusion criteria for the studies are as follows:

  1. Type of study: We only included randomized controlled trials published in Chinese or English to examine the efficacy of PA on CRF. PA has been defined as any bodily movement generated by skeletal muscles that need energy consumption by the World Health Organization (Okely et al., 2021). According to the available literature (Huang et al., 2022), the modes of PA were divided into four types: aerobic exercise, resistance exercise, mixed mode or other exercise.

  2. Type of participant: Patients diagnosed with colorectal cancer were included. We imposed no restrictions on age, sex, race or time to start the intervention. Considering the inclusion of patients with metastatic disease is likely to contaminate results, patients with distant metastatic CRC or any conditions affecting movement were excluded but were eligible regardless of whether they were pre‐, during or following treatment. Studies involving participants with different types of cancer were included only if the results were reported separately for participants with CRC.

  3. Type of intervention: All forms of PA were included. We imposed no restrictions on the type, intensity or frequency of exercise. Studies were excluded if the experimental group in this study had combined exercise training with another interventions (e.g. pharmaceutical or nutrition interventions) and the intervention group only increases PA relative to the control group.

  4. Outcomes: Fatigue. Fatigue should be evaluated by a validated fatigue questionnaire.

  5. Type of control group: Routine care group or blank control group (only usual care with no PA interventions or structured exercise prescription).

Studies were excluded if they were comments, descriptive studies, protocols, conference abstracts, dissertations, qualitative studies and editorials. Studies that were duplicates and the full text not available were also excluded.

2.3. Study selection

NoteExpress3.2.0 was used to remove duplicates of the citations of all searched studies. After that, two authors independently screened the whole citations and determined if they met the inclusion criteria based on the title, abstracts or full‐text articles. The two reviewers discussed about the eligibility until they achieved consensus on the eligible studies. The detailed study selection process is summarized in Figure 1.

FIGURE 1.

FIGURE 1

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Flow diagram of article identification and selection.

2.4. Methodological quality appraisal

The ROB1 developed by the Cochrane Collaboration was used for assessing the risk of bias in randomized controlled trials, which included seven domains (Higgins et al., 2011). Since it was not possible to perform blinding of patients and key personnel blinding, we only assessed blinding according to the domain of detection bias. The quality appraisal of the included studies was evaluated by two reviewers independently, and it is necessary for a third author to recheck the outcome until an agreement was reached through discussion if there was a discrepancy.

2.5. Data extraction and synthesis

For the included trials, the following information was extracted by two independent authors using a structured form: general information (title, authors, country and year of publication), study characteristics (sample, inclusion and exclusion criteria), patient characteristics (age, gender, time since surgery and current treatment), intervention and control characteristics (mode/type, intensity, frequency, time/duration and programme length), outcome measures, the questionnaires and limitations. The selection of intervention and control characteristics followed the principle of FITT (frequency, intensity, type and time) based on the American College of Sports Medicine (ACSM) exercise guidelines (Thompson et al., 2013). Any disagreement between the two authors was solved by discussion or verification through the third author. The numerical outcome data of the two included studies were missing, such as Pinto et al. (2013) reported 95% confidence intervals for post‐intervention values instead of standard deviations and Brown et al. (2018) only reported the change‐from‐baseline value scores. We emailed to request original post‐intervention data, but did not receive a response. To reduce the loss of information and publication bias, we finally transformed the data under the guidance of the Cochrane Handbook for Systematic Reviews of Interventions (Higgins et al., 2022).

2.6. Statistical analysis

RevMan5.4 software was used for performing meta‐analysis. For continuous data, mean differences (MDs) or standardized mean differences (SMDs) combined with a 95% confidence interval (CI) was used to evaluate the efficacy of PA for CRF, and it was considered statistically significant when p < 0.05. Heterogeneity among the included studies was tested by chi‐square test, for example, if the heterogeneity among the results is acceptable (p > 0.1, I 2 < 50%), the fixed effect model was used for meta‐analysis; if there is large heterogeneity among studies (p ≤ 0.1, I 2 ≥ 50%), random effect model was used. Thanks to the relationship of dose–response that exists in entire kinds of PA and the high heterogeneity of the included studies, we performed subgroup analyses based on the recommendation of clinical guidelines for exercise mode and weekly duration (<150 min/per week, ≥150 min/week); length (<6 months, ≥6 months); mode (aerobic, resistance, multicomponent or other, e.g. yoga, Baduanjin) (Okely et al., 2021). When the number of studies included in each separate meta‐analysis was more than or equal to 3, we also performed a sensitivity analysis by excluding individual studies one by one to test the robustness of the results.

3. RESULTS

3.1. Study selection

The process of comprehensive search and article selection are summarized in Figure 1. 3356 citations were identified through seven databases and other sources totally, and 969 of them were removed due to duplicates. Then, 2251 records were removed because they obviously did not meet the inclusion criteria by reading the title and abstract, leaving 142 full‐text articles to be verified for eligibility, eight articles were included for data extraction and the final systematic review (Brown et al., 2018; Cramer et al., 2016; Kim et al., 2019; Lu et al., 2019; Pinto et al., 2013; Van Vulpen et al., 2016; Weiying & Suxia, 2014; Xiuli et al., 2018).

3.2. Methodological quality of the included studies

The result of the risk of bias assessment for the identified RCTs was depicted in Figure 2. Generally, the methodological quality of the included studies is moderate. The method of randomization was reported by seven articles, but only one study conducted allocation concealment by preparing sealed and non‐transparent envelopes (Cramer et al., 2016). Van Vulpen et al. (2016) and Cramer et al. (2016) also performed blinding for the assessor. Five different studies declared the details about conflict of interest (Brown et al., 2018; Cramer et al., 2016; Kim et al., 2019; Lu et al., 2019; Van Vulpen et al., 2016), and four studies disclosed funding source (Brown et al., 2018; Kim et al., 2019; Pinto et al., 2013; Van Vulpen et al., 2016). Three trials have been registered prospectively (Brown et al., 2018; Lu et al., 2019; Van Vulpen et al., 2016) and all articles described the information of ethics committee approval.

FIGURE 2.

FIGURE 2

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Risk of bias assessment of the randomized controlled trials.

3.3. Study characteristics of the included studies

3.3.1. Patient characteristics

The characteristics of the eight articles are presented in Table 1. The studies were conducted in five countries: China (n = 3), Germany (n = 1), Korea (n = 1), the United States (n = 2) and the Netherlands (n = 1). Generally, our study enrolled 542 CRC survivors and all enrolled participants were in the period of 5 years after surgery. Three identified studies included patients with CRC undergoing adjuvant chemotherapy (Lu et al., 2019; Van Vulpen et al., 2016; Weiying & Suxia, 2014), and two studies included CRC survivors who finished the whole of treatments (Brown et al., 2018; Pinto et al., 2013).

TABLE 1.

Characteristics of the included randomized controlled trials.

Author, year Country Setting Sample size/age (year)/sex (male (M); female (F)) Stage of cancer/status Exercise modes (intervention (I)/control (C)) Length of intervention (L)/Exercise adherence (A) (%) Weekly duration of exercise (min/week) Instrument for CRF measurement CRF results
Brown et al. (2018) USA Community

Control

n = 13 (M = 4, F = 9)

Low‐dose

n = 14 (M = 7, F = 7)

High‐dose

n = 12 (M = 4, F = 8)

Age: NA

 I–III; Completed cancer treatment(s) within 36 months of entering the study

I: running

C: care as usual

L = 6 months

Low‐dose: A = 93 ± 2%

High‐dose: A = 89 ± 3%

Low‐dose: 150

High‐dose: 300

 FSI

Control

Pre = 6.9 ± 11.9

Pos = 0.1 ± 6.1237/6.6144

Low‐dose

Pre = 3.8 ± 7.2

Pos = 0.9 ± 8.9814

High‐Dose 0.90.1

Pre = 12.7 ± 17.2

Pos = −5.9 ± 9.0067
Van Vulpen et al. (2016) Netherlands Not mentioned

Control

n = 16 (M = 11, F = 5)

Age = 58.1 ± 9.6

Intervention

n = 17 (M = 10, F = 7)

Age = 58.1 ± 10.3

 M0; undergoing Chemotherapy

I: aerobic and muscle strength training

C: care as usual

L = 18 weeks

A = 89%

 ≥210 MFI NA
Cramer et al. (2016) Germany Community

Control

n = 27 (M = 16, F = 11)

Age = 67.81 ± 10.37

Intervention

n = 27 (M = 17, F = 10)

Age = 68.70 ± 9.13

 I–III; 2–48 months post‐surgery

I: yoga

C: care as usual

L = 10 weeks

A: NA

 90 FACIT‐F

Control

Pre = 40.13 ± 7.72

Pos = 40.45 ± 8.04

Intervention

Pre = 42.70 ± 9.19

Pos = 43.02 ± 6.52
Weiying and Suxia (2014) China Hospital and community

Control

n = 60 (M = 37, F = 23)

Age = 58.9 ± 5.12

Intervention

n = 60 (M = 41, F = 19)

Age = 56.2 ± 6.01

 Undergoing Chemotherapy, 2–3 weeks post‐surgery

I: walking

C: care as usual

L = 4 weeks

A: NA

 75 BFI

Control

Pre = 2.41 ± 0.52

Pos = 6.30 ± 1.18

Intervention

Pre = 2.36 ± 0.56

Pos = 5.01 ± 1.12
Kim et al. (2019) Korea Community

Control

n = 34 (M = 17, F = 17)

Age = 56.8 ± 10.2

Intervention

n = 37 (M = 18, F = 19)

Age = 55.7 ± 8.7

 II–III; completed all standard surgery and adjuvant chemotherapy within 4 weeks–2 years

I: aerobic and resistance training

C: care as usual

L = 12 weeks

A: NA

 ≥210 FACIT‐F

Control

Pre = 41.00 ± 8.10

Pos = 42.30 ± 7.50

Intervention

Pre = 39.70 ± 9.60

Pos = 42.60 ± 8.50
Lu et al. (2019) China Hospital and community

Control

n = 44 (M = 30, F = 14)

Age = 54.63 ± 11.88

Intervention

n = 43 (M = 26, F = 17)

Age = 55.60 ± 11.23

 I–III; undergoing chemotherapy

I: Baduanjin qigong

C: care as usual

L = 24 weeks

A: NA

 ≥100 BFI

Control

Pre = 4.70 ± 2.50

3 months = 4.40 ± 2.40

6 months = 4.10 ± 1.90

Intervention

Pre = 4.40 ± 2.20

3 months = 4.30 ± 2.10

6 months = 2.70 ± 2.10
Pinto et al. (2013) USA Community

Control

n = 24 (M = 12, F = 14)

Age = 55.6 ± 8.24

Intervention

n = 19 (M = 8, F = 12)

Age = 59.5 ± 11.2

 I–III; ≤5 years since treatment completion

I: Brisk walking, biking, or use of home exercise equipment

C: care as usual

L = 12 weeks

A: NA

 ≤150 FACT‐F

Control

Pre = 37.9 ± 10.6

Pos = 41.9 ± 5.8

Intervention

Pre = 40.7 ± 8.7

Pos = 42.2 ± 6.1
Xiuli et al. (2018) China Hospital and community

Control

n = 47 (M = 21, F = 29)

Age = 50.6 ± 6.2

Intervention

n = 48 (M = 20, F = 30)

Age = 51.3 ± 5.8

 After surgery

I: walking

C: care as usual

L = 6 months

A: NA

 ≤100 RPFS

Control

Pre = 4.83 ± 2.64

Pos = 5.25 ± 1.64

Intervention

Pre = 4.82 ± 3.33

Pos = 4.13 ± 2.78
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3.3.2. Characteristics of PA interventions

The PA interventions included fitness activities, sports activities and skills activities, such as jogging (Weiying & Suxia, 2014), cycling (Brown et al., 2018), swimming (Kim et al., 2019), running (Brown et al., 2018), muscle strength training (Van Vulpen et al., 2016), walking (Kim et al., 2019; Pinto et al., 2013; Weiying & Suxia, 2014; Xiuli et al., 2018), yoga (Cramer et al., 2016) and Baduanjin Qigong (Lu et al., 2019). Six of the included trials performed aerobic exercises for the intervention group (Brown et al., 2018; Cramer et al., 2016; Lu et al., 2019; Pinto et al., 2013; Weiying & Suxia, 2014; Xiuli et al., 2018), two trials performed aerobic exercise combined with resistance exercise (Kim et al., 2019; Van Vulpen et al., 2016), but no trials involved resistance exercise only. The setting of the included studies contained hospital and community, and the majority of the interventions used moderate‐intensity aerobic exercise.

Notably, participants who had the habit of regular exercise were excluded in two of the included studies (Brown et al., 2018; Weiying & Suxia, 2014) and all studies imposed no restrictions on doing exercise for the control group during the intervention. The control groups of the study by Cramer et al. (2016) and Van Vulpen et al. (2016) were selected on a waiting list, and patients were suggested to take part in exercise programmes after the PA interventions due to ethical reasons (Cramer et al., 2016; Van Vulpen et al., 2016). Some identified studies also provided practical support by providing weekly phone counsel (Brown et al., 2018; Kim et al., 2019; Pinto et al., 2013), checking their exercise log (Lu et al., 2019), providing small group training sessions or videos (Kim et al., 2019; Lu et al., 2019). In addition, only one study took the mention the adverse events (Cramer et al., 2016), and five studies described the reason for dropout (Cramer et al., 2016; Kim et al., 2019; Lu et al., 2019; Van Vulpen et al., 2016; Xiuli et al., 2018).

3.3.3. Characteristics of CRF measures

Cancer‐related fatigue was measured by six different questionnaires, such as the Functional Assessment of Chronic Illness Therapy–Fatigue (FACIT‐F) (Cramer et al., 2016; Kim et al., 2019), Functional Assessment of Cancer Therapy Scale–Fatigue (FACT‐F) (Pinto et al., 2013), Revised Piper Fatigue Scale (RFPS) (Xiuli et al., 2018), Brief Fatigue Inventory (BFI) (Lu et al., 2019; Weiying & Suxia, 2014), Multidimensional Fatigue Inventory (MFI) (Van Vulpen et al., 2016) and Fatigue Symptom Inventory (FSI) (Brown et al., 2018). The instrument for CRF measurement and fatigue outcomes of eight studies are presented in Table 1, and it showed a statistical difference between the two groups only in five studies, although a decreasing trend of fatigue triggered by exercise was found in all studies.

3.4. Meta‐analysis of the effects of physical activity

3.4.1. Overall analysis of the effects of physical activity

Due to the different types of questionnaires used and high heterogeneity (p = 0.01, I 2 = 62%), we chose the SMD and random‐effects model to perform an overall meta‐analysis of the effects of PA for CRF (Figure 3), and it showed a statistical difference between the two groups (SMD = −0.46; 95% CI: [−0.76, −0.15], Z = 2.93 and p = 0.003). Sensitivity analysis showed that no statistically significant changes were found in the combined effects after excluding single study results one by one (SMD ranged from −0.35 [95% CI: −0.57 to −0.13] to −0.53 [95% CI: −0.85 to −0.23], I 2 ranged from 12% to 70%).

FIGURE 3.

FIGURE 3

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Forest plot of effect of exercise on cancer‐related fatigue.

3.4.2. Subgroup analysis for the length of intervention: ≥6 months vs <6 months

A total of four studies with a length of intervention less than but not equal to 6 months and three studies with a length of intervention lasting for at least 6 months were included for subgroup analysis (Figure 4). Random‐effects model was used due to the high heterogeneity (p = 0.01, I 2 = 62%). And the results revealed that there were no statistically significant effects for CRF when the length of the intervention was less than but not equal to 6 months (SMD = −0.41; 95% CI: [−0.97, 0.16], Z = 1.42, p = 0.16), on the contrary, CRF was significantly improved when the length of the intervention was at least 6 months (SMD = −0.54; 95% CI: [−0.81, −0.27], Z = 3.87, p = 0.0001). The results of sensitivity analyses for both the subgroups reflected that no individual study could change the results (SMD ranged from −0.14 (95% CI: −0.44 to 0.17) to −0.53 (95% CI: −1.20 to 0.13), I 2 ranged from 0% to 87%; SMD ranged from −0.44 (95% CI: −0.79 to −0.09) to −0.58 (95% CI: −0.88 to −0.29), I 2 ranged from 0% to 10%).

FIGURE 4.

FIGURE 4

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Forest plot of subgroup analysis for length of intervention: ≥6 months vs <6 months.

3.4.3. Subgroup analysis for weekly duration of exercise: ≥150 min/week vs <150 min/week

A total of three studies with a weekly duration of intervention less than but not equal to 150 min/week and two studies with a weekly duration of intervention reaching up to at least 150 min/week were included for subgroup analysis (Figure 5). Random‐effects model also was used in both the two subgroups due to the high heterogeneity (p = 0.009, I 2 = 67%). When patients exercised for less than but not equal to 150 min/week, PA significantly reduced CRF, however, PA had no effect on CRF when patients exercised for more than 150 min/week (SMD = −0.67; 95% CI: [−1.15, −0.19], Z = 2.74, p = 0.006; SMD = −0.12; 95% CI: [−0.50, 0.26], Z = 0.61 and p = 0.54). And sensitivity analysis showed that the result of the subgroup analysis was stable (SMD ranged from −0.43 [95% CI: −0.76 to −0.11] to −0.80 [95% CI: −1.42 to −0.19], I 2 ranged from 0% to 81%).

FIGURE 5.

FIGURE 5

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Forest plot of subgroup‐analysis for weekly duration of exercise: ≥150 min/week vs <150 min/week.

3.4.4. Analysis of exercise mode

Since the quantity of studies on different exercise modes was too small, we performed a narrative summary instead of a subgroup analysis. Overall, four trials adopted aerobic exercise interventions only (Brown et al., 2018; Pinto et al., 2013; Weiying & Suxia, 2014; Xiuli et al., 2018), and three of them showed improvements in fatigue (Brown et al., 2018; Weiying & Suxia, 2014; Xiuli et al., 2018). Two trials conducted aerobic exercise combined with resistance exercise intervention among CRC patients (Kim et al., 2019; Van Vulpen et al., 2016), but only one of them have a positive outcome (Van Vulpen et al., 2016). And there were no studies using resistance exercise alone as an intervention. As for the other mode of exercise, the result of a Baduanjin Qigong Exercise programme indicated that Baduanjin can significantly relieve CRF (Lu et al., 2019). However, a 10 weeks yoga intervention programme did not reduce fatigue (Holger Cramer et al., 2016).

4. DISCUSSION

To the best of our knowledge, this review is the first to examine the content and efficacy of PA for CRF among CRC survivors. Eight RCTs with a total of 542 patients were included for quantitative analysis, and the result of the meta‐analysis, in accordance with previous studies (Dun et al., 2020; Machado et al., 2022; Singh et al., 2020), indicated that PA showed significantly on reducing fatigue for CRC survivors. Several longitudinal studies have also confirmed a significant correlation between PA and CRF: the lower the level of exercise in patients, the higher the level of fatigue (Hodges et al., 2022; Winters‐Stone et al., 2008). It is hypothesized that the possible mechanism that explains why PA reduces CRF is that exercise can enhance cardiopulmonary function, improve blood circulation, promote the metabolism of the body and boost immunity by increasing haemoglobin levels and improving peak oxygen uptake, thus, alleviating the symptoms of CRF eventually (Hussey & Gupta, 2022; Zhu et al., 2022). Therefore, encouraging and coaching cancer patients to be more physically active is of clinical relevance. It is also worth noting that, due to the complex aetiology of fatigue and frequent appearance in the form of symptom clusters, CRF may persist even in patients recovering from well‐controlled cancer after a series of rehabilitative treatments such as correction of anaemia (Campos et al., 2011), which fully reflects the complexity of CRF, hence, clinical staff should follow the fatigue management guidelines, assess the causes of fatigue and integrate other interventions flexibly with PA interventions to maximize the improvement of CRF and quality of life.

We also found that sticking to PA for at least 6 months was more effective than sticking to PA for less than 6 months, which may be related to the mechanism of over‐recovery, that is, the effect of exercise on fatigue probably goes through a process of ‘load‐fatigue‐recovery‐over‐recovery’. In brief, this is a phenomenon in which the patient's fatigue level rises and then falls below the original level through appropriate exercise training. If the intervention period is too short, the over‐recovery cannot be achieved, thus, the effect of PA intervention will be affected. For example, Lu et al. (2019) who conducted a Baduanjin Qigong Exercise programme, revealed that there were significant group differences not at 3 months but at 6 months. According to previous studies, a long‐term exercise intervention is also associated with an increase in QoL, aerobic fitness and reduced body fat (Singh et al., 2020). Therefore, sticking to PA also may be one of the key factors in reducing fatigue. Notably, PA started within 6 months after surgery seems to be more effective than PA started 6 months after surgery, and on account of the low number of studies in our systematic review, which may be a chance finding. One explanation could be that early fatigue management is more helpful for fatigue relief.

With respect to the weekly duration of exercise, it has been recommended that people living with chronic conditions should undertake a goal of 150 min/week of moderate‐intensity exercise in most international health guidelines (Okely et al., 2021). Previous studies also investigated the optimal weekly duration of PA needed. For instance, Brown et al. (2018) performed a randomized three‐arm exercise trial among CRC survivors and also found that it was a significant improvement in fatigue in the 300 min/week of exercise group other than the control or 150 min/week of exercise groups. Results from a national longitudinal cohort study of 88,140 US adults also showed that 150–300 min/week of exercise reduced the risk of cancer‐specific mortality by 24%, and the protective effect of PA on cancer‐specific mortality increased with increasing levels of PA (Zhao et al., 2019). Consequently, a high level of aerobic exercise may be necessary for reducing fatigue. However, in our study, it is surprising to find that PA intervention has a significant improvement in CRF when patients exercised for less than 150 min/week, rather than more than 150 min/week. There are several possible explanations for the different results. First, notably, some studies have suggested that the starting level of exercise recommended by some guidelines may be too high for cancer survivors, especially those with CRF, psychological disorders or chronic pain, and it is known that a long‐term low to moderate levels of exercise is sufficient to maintain continued health benefits (Piercy et al., 2018). For example, a meta‐analysis that included 75 studies demonstrated that exercise interventions of less than 120 min/week can achieve optimal pain‐improving effects (Polaski et al., 2019), so assessing the optimal weekly duration of exercise for fatigue critically is necessary. Second, the correlation between the dose–response association and the type of exercise has been demonstrated (Gallardo‐Gómez et al., 2022), which means that different types of exercise may have different efficacy on CRF even if the dose of exercise is the same. However, further subgroup analysis could not be performed because the number of included studies was too small in our study, hence, it is somewhat unreasonable to analyse the effect of different weekly duration of exercise on CRF without taking into account the effect of different exercise types or intensity. Besides, we observed that fatigue levels in the studies included in this subgroup analysis were considerably lower at the baseline and participants were high functioning (Brown et al., 2018; Kim et al., 2019), hence, demonstrating that more than 150 min/week of exercise is effective for fatigue may be impossible due to the ceiling effects. In addition, only two studies reported contamination rates and most of the researchers imposed no restrictions on exercise for the control group, which may also lead to high exercise contamination as the usual care group may continue to be physically active during the intervention (Lin et al., 2014). A systematic review also reported that the levels of contamination were occasionally high in PA trials (Burn et al., 2019), indicating that contamination may be a meaningful problem and needs more attention. Last but not least, the high dropout rate and small sample size of some included studies is also an important limitation, which might reduce the confidence in the intention‐to‐treat analysis and the robustness of the subgroup analysis.

Our results also show that aerobic exercise, aerobic exercise combined with resistance exercise and other modes of exercise may be all effective in improving fatigue, which is consistent with the previous studies. For instance, a network meta‐analysis that included a total of 245 RCTs found that aerobic exercise, aerobic exercise combined with resistance exercise, resistance exercise and yoga can significantly improve the CRF (Hilfiker et al., 2018). However, in our study, there were no significant differences between the two groups in the PA programme of Hatha yoga. The lower adherence rate may have contributed to this result as nearly half of the participants in the exercise group failed to complete their sessions. Taken together, the efficacy of different modes of exercise on CRF and what is the optimal exercise type are still uncertain in CRC survivors, hence, more high‐quality studies are needed to evaluate the efficacy of these modes of PA on CRF. The last thing to emphasize is that it is known that doing some PA is better than doing none according to the WHO guideline (Bull et al., 2020) and several studies have also demonstrated that there is no minimum threshold for the benefits of exercise (Gallardo‐Gómez et al., 2022), consequently, decision‐makers involved in health policies should consider PA interventions as effective measures for CRF management and recommend it to more CRC survivors.

Some common issues deserve noting with respect to the risk of bias for identified studies, such as the absence of a description of random sequence generation, allocation concealment, blinding of personnel and outcome assessment, adherence and dropout rates of the participants. In addition, the intention‐to‐treat analyses have been used in a few of the included studies, which may reduce the stability of the outcome, hence, these methodological problems should be avoided as much as possible in future research and the findings of studies should be reported in deference to the corresponding reporting guidelines.

5. STRENGTHS AND LIMITATIONS

The strength of this study is that all eight included studies met the requirement of “the intervention group only increases PA relative to the control group”, which will be more conducive to observing the effect of PA intervention. Additionally, compared with previous relevant studies, we included more studies, which is beneficial for performing subgroup analysis to compare the content and efficacy of PA interventions on fatigue.

This study has several limitations. The number of studies included in our study was small, which was not beneficial for obtaining more convincing results, thus, the conclusions of this study should be interpreted cautiously. Second, the heterogeneity of the results of this study is high, possibly due to the following reasons: (1) patients at different stages of the disease: some studies recruited patients undergoing postoperative adjuvant chemotherapy, while others included CRC patients who have completed all the treatment for several years; (2) the modes of PA, weekly duration of exercise and length of the programme were different: some studies chose single aerobic exercise, some studies chose aerobic exercise combined with resistance exercises, some studies chose more than 210 min/week, some studies required only 75 min/week and some studies continued the programme for more than 6 months, while some only lasted a few weeks; (3) different scales were selected: for example, the RPFS scale was adopted in some studies, and the FSI scale was used in others, with varied scales may result in differences in data consolidation. In addition, it was unreliable for the robustness of the outcome on account of the small sample size of some identified studies, thus, more large RCTs should be carried out in the future to examine the efficacy and content of PA on fatigue among CRC patients.

6. CONCLUSION

In conclusion, exercise for at least 6 months and less than 150 min/week were effective in reducing fatigue among CRC survivors. Aerobic exercise was probably a key factor affecting the results, and future research should further verify the optimal mode of exercise, volumes of exercise and when is the best time to initiate a PA intervention for CRC patients.

AUTHOR CONTRIBUTIONS

Liangrong Geng and Xiaoyu Li: Systematic review protocol design and article writing; Xiaoyu Li, Liqun Guo and Rui Zhang: Selection of original studies and data extraction analysis; Shujin Yue: Revision of the draft and supervision of the research. Consensus was reached on the content of the article and submission by all authors.

FUNDING INFORMATION

This study was supported by the Fundamental Research Funds for the Central Universities [2022‐JYB‐JBZR‐026].

CONFLICT OF INTEREST STATEMENT

The authors have no funding or conflicts of interest to disclose.

ETHICAL APPROVAL

It was not applicable due to the types of this study.

PATIENT CONSENT STATEMENT

It was not required due to the types of this study.

ACKNOWLEDGEMENTS

The authors have no acknowledgements to make.

Geng, L. , Li, X. , Guo, L. , Zhang, R. , & Yue, S. (2023). The content and effectiveness of physical activity for cancer‐related fatigue among colorectal cancer survivors: Systematic review and meta‐analysis. Nursing Open, 10, 4274–4285. 10.1002/nop2.1725

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