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REVIEW ARTICLE (META-ANALYSIS)|Articles in Press
Effectiveness of Therapeutic Exercise Models on Cancer-Related Fatigue in
Patients With Cancer Undergoing Chemotherapy: A Systematic Review and Network
Meta-analysis
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EFFECTIVENESS OF THERAPEUTIC EXERCISE MODELS ON CANCER-RELATED FATIGUE IN
PATIENTS WITH CANCER UNDERGOING CHEMOTHERAPY: A SYSTEMATIC REVIEW AND NETWORK
META-ANALYSIS

 * Aida Herranz-Gómez, MSc
   Aida Herranz-Gómez
   Affiliations
   Department of Physiotherapy, Faculty of Health Sciences, European University
   of Valencia, Valencia, Spain
   
   
   
   Exercise Intervention for Health Research Group (EXINH-RG), Department of
   Physiotherapy, University of Valencia, Valencia, Spain
   Search for articles by this author
 * Ferran Cuenca-Martínez, PhD
   Ferran Cuenca-Martínez
   Correspondence
   Corresponding author: Dr Ferran Cuenca Martínez, C/Gascó Oliag 5, Department
   of Physiotherapy, University of Valencia, 46010 Valencia, Spain.
   Contact
   Affiliations
   Exercise Intervention for Health Research Group (EXINH-RG), Department of
   Physiotherapy, University of Valencia, Valencia, Spain
   Search for articles by this author
   
 * Luis Suso-Martí, PhD
   Luis Suso-Martí
   Affiliations
   Exercise Intervention for Health Research Group (EXINH-RG), Department of
   Physiotherapy, University of Valencia, Valencia, Spain
   Search for articles by this author
 * Clovis Varangot-Reille, MSc
   Clovis Varangot-Reille
   Affiliations
   Centre Hospitalier Lyon Sud, Hospices Civils de Lyon, Pierre-Bénite, Lyon,
   France
   Search for articles by this author
 * 
 * Miriam Prades-Monfort, PT
   Miriam Prades-Monfort
   Affiliations
   Exercise Intervention for Health Research Group (EXINH-RG), Department of
   Physiotherapy, University of Valencia, Valencia, Spain
   Search for articles by this author
 * Joaquín Calatayud, PhD
   Joaquín Calatayud
   Affiliations
   Exercise Intervention for Health Research Group (EXINH-RG), Department of
   Physiotherapy, University of Valencia, Valencia, Spain
   Search for articles by this author
 * Jose Casaña, PhD
   Jose Casaña
   Affiliations
   Exercise Intervention for Health Research Group (EXINH-RG), Department of
   Physiotherapy, University of Valencia, Valencia, Spain
   Search for articles by this author
 * Show all authors

Open AccessPublished:January 31,
2023DOI:https://doi.org/10.1016/j.apmr.2023.01.008
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HIGHLIGHTS

 * •
   During chemotherapy, aerobic and/or resistance exercise showed a positive
   trend compared with flexibility exercise showed a positive trend in reducing
   cancer-related fatigue.
 * •
   Aerobic and/or resistance exercise also showed favorable trends versus usual
   care alone when these exercise types are instituted during chemotherapy.


ABSTRACT


OBJECTIVE

To assess and compare the effectiveness of different exercise modalities in
reducing cancer-related fatigue (CRF) in patients with cancer undergoing
chemotherapy. Exercise intensities for selected exercise types were also
compared.


DATA SOURCES

We conducted a search in MEDLINE, Embase, CINAHL, Scopus, SPORTDiscus, and Web
of Science from inception to October 15, 2021.


STUDY SELECTION

Randomized controlled trials concerning the effectiveness of exercise modalities
on CRF in patients with cancer undergoing chemotherapy were included.


DATA EXTRACTION

Study characteristics were extracted using a structured protocol. Methodological
quality was assessed employing the PEDro scale and risk of bias was assessed
using the Revised Cochrane Risk of Bias Tool for Randomized Trials. The
certainty of evidence was assessed based on Grading of Recommendations,
Assessment, Development and Evaluation. The measure of effect used was the
adjusted standardized mean difference (SMD) or Hedge's g, together with the
corresponding 95% confidence intervals (CI).


DATA SYNTHESIS

Forty-seven studies were included. Data were pooled employing a random-effects
model. There was a trend that adding low-intensity aerobic and resistance
exercise (SMD=1.28, 95% CI -0.18; 2.75, P=.086), or moderate-intensity aerobic
and resistance exercise (SMD=0.85; 95% CI -0.12; 1.82, P=.087), was more
effective than adding flexibility training to usual care (UC). There was also a
trend that UC alone was less effective than adding moderate-intensity aerobic
and resistance exercise (SMD=-0.47, 95% CI -0.96, 0.02, P=.060) to UC.


CONCLUSIONS

The addition of low- to moderate-intensity aerobic and/or resistance exercise
demonstrated a positive trend for improvement in CRF in patients with cancer
undergoing chemotherapy, when compared with UC alone or UC with flexibility
training.


KEYWORDS

 * Chemotherapy
 * Exercise therapy
 * Fatigue
 * Medical oncology
 * Rehabilitation

LIST OF ABBREVIATIONS:

CI (confidence intervals), CRF (cancer-related fatigue), GRADE (Grading of
Recommendations, Assessment, Development and Evaluation), HIIT (high-intensity
interval training), κ (Kappa coefficient), MICT (moderate-intensity continuous
training), RCT (randomized controlled trials), SMD (standardized mean
difference), UC (usual care)

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Screening, assessment, and management of fatigue in adult survivors of cancer:
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Comparison of pharmaceutical, psychological, and exercise treatments for
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Pharmacological interventions include psychostimulants or other wakefulness
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Screening, assessment, and management of fatigue in adult survivors of cancer:
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Comparison of pharmaceutical, psychological, and exercise treatments for
cancer-related fatigue: a meta-analysis.
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All interventions have been shown to improve the CRF. Exercise modalities
provide a slightly larger improvement, followed by psychological interventions
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effect sizes and 95% confidence intervals (CI) of 0.30 (0.25; 0.36), 0.27 (0.21;
0.33), and 0.26 (0.13; 0.38), respectively.
16
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 * et al.

Comparison of pharmaceutical, psychological, and exercise treatments for
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Pharmacological treatment produced a more modest improvement of 0.09 (0.00;
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16
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Comparison of pharmaceutical, psychological, and exercise treatments for
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However, there is no clear consensus on the concrete clinical implementation of
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presence of severe CRF before treatment, but physical activity before and during
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Despite the guidelines showing that exercise has good results on CRF during
oncology treatment, we cannot give the patient a precise answer as to what type
of exercise would be most beneficial to them alongside their chemotherapy.
Therefore, the aim of this systematic review and network meta-analysis was to
compare the effectiveness of different exercise modalities in reducing CRF in
patients with cancer undergoing chemotherapy.


METHODS


PROTOCOL AND REGISTRATION

This systematic review and network meta-analysis was conducted in accordance
with the Preferred Reporting Items for Systematic Reviews incorporating Network
Meta-Analysis (PRISMA-NMA) extension statement.
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The protocol of this study was registered in an international register prior to
starting the review (PROSPERO, CRD42022292706).


ELIGIBILITY CRITERIA

The selection criteria for the systematic review were based on methodological
and clinical factors such as population, intervention, comparison, outcomes, and
study design criteria.
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POPULATION

Patients with cancer over 18 years of age and undergoing chemotherapy were
included. Patients could have received or be scheduled to receive other
treatments such as surgery, as long as they included chemotherapy. There was no
restriction by sex, type and stage of cancer, or type of chemotherapy.

INTERVENTION AND COMPARISON

All patients in the study received first-choice chemotherapy. The study had to
include at least 1 arm that included exercise during chemotherapy treatment (eg,
aerobic, resistance, or flexibility exercise). We included studies that
implemented the exercise session before, during, or after the chemotherapy
session, as well as between chemotherapy sessions.

OUTCOMES

Studies were included if they assessed CRF and presented data from baseline,
post-intervention and/or short-, medium-, and/or long-term follow-up assessment.
When CRF was assessed with more than 1 questionnaire, we selected the 1
presented as the primary outcome. Studies had to present the data derived from
the analyses, represented numerically and/or graphically.

STUDY DESIGN

Randomized controlled trials (RCTs) (including pilot RCT) were included. There
was no restriction based on date, publication status, or any specific language
as recommended by international criteria.
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SEARCH STRATEGY

We searched for scientific articles in the MEDLINE (PubMed), Embase, Cumulative
Index to Nursing and Allied Health Literature (CINAHL), Scopus, SPORTDiscus, and
Web of Science databases from inception to October 15, 2021. Databases were
reviewed prior to statistical analysis to identify additional articles published
up to January 15, 2022. We manually checked the reference sections of included
studies, checked studies included in reviews related to the topic and contacted
authors for additional information where necessary. We also use the Connected
papers website, which displays articles according to their similarity (based on
co-citation and bibliographic linking).
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The search was adapted and performed in Google Scholar. The search strategy is
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SELECTION CRITERIA

The identified references were exported to the Rayyan QCRI software, used to
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study questions and objectives using information from the study title, abstract,
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sufficient information. In the second phase, we assessed the full text of each
study for compliance with the inclusion criteria. The article selection process
was conducted by 2 independent researchers (A.H.G. and C.V.R.) and differences
were resolved by consensus moderated by a third researcher (F.C.M.).
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DATA EXTRACTION AND EFFICACY MEASURES

Two independent researchers (A.H.G. and M.P.M.) extracted study characteristics
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information was obtained from each study.
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Exercise modalities were categorized as aerobic exercise, resistance exercise,
flexibility exercise (including stretching), high-intensity interval training
(HIIT) or moderate-intensity continuous training (MICT), yoga, light martial
arts (including qigong or taichi). In aerobic and resistance exercise, intensity
was categorized as low, moderate, or high according to the reference values for
percentage of heart rate reserve, maximum heart rate, or maximal oxygen
consumption, indicated by the American College of Sports Medicine's Guidelines
for Exercise Testing and Prescription (ie, moderate-intensity corresponded with
40%-59% of heart rate reserve or oxygen uptake reserve or 64%-76% of maximal
heart rate or 46%-63% maximum oxygen consumption; high-intensity corresponded
with 60%-89% of heart rate reserve or oxygen uptake reserve, or 77%-95% of
maximal heart rate or 64%-90% maximum oxygen consumption).
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Systematic Reviews of Interventions version 6.2: SD=√(N)*(upper limit – lower
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referred to the same sample of patients with cancer were considered only once,
in order to reduce bias in the results.


METHODOLOGICAL QUALITY AND RISK OF BIAS ASSESSMENT

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(8) fewer than 15% dropouts; (9) intention-to-treat analysis; (10) between-group
statistical comparisons; and (11) point measures and variability data. Each
criteria were scored as yes (1 point) or no/unknown (0 points). The PEDro score
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(9-10=excellent; 6-8=good; 4-5=fair; 3-0=poor).
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bias for each trial.
Two independent reviewers (A.H.G. and M.P.M.) assessed methodological quality
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researcher (F.C.M.). We calculated the linear weighted Cohen's kappa coefficient
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OVERALL STRENGTH OF THE EVIDENCE

We evaluated the certainty of evidence analysis based on classifying the results
into levels of evidence according to the Grading of Recommendations, Assessment,
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for network meta-analyses from Salanti et al: study design, imprecision,
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Supplemental Table B.1 shows the characteristics of the included RCTs
(demographic characteristics, interventions, outcomes, and study design).


STUDY CHARACTERISTICS

A total of 4056 participants were included in 47 studies. Some studies referred
to the same population, assessed at different time points,
59
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85
 * Mijwel S
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into breast cancer survivorship.
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this was taken in account when calculating the total sample. The mean age of the
included population was 52.6±11.3 and 82.1% of the sample were women.
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cancer,
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cancer.
Med Sci Sports Exerc. 2021; 53: 496-505
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 * Google Scholar

,
76
 * Hornsby WE
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Safety and efficacy of aerobic training in operable breast cancer patients
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,
77
 * Husebø AML
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Effects of scheduled exercise on cancer-related fatigue in women with early
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,
80
 * Kirkham AA
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Chemotherapy-periodized” exercise to accommodate for cyclical variation in
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Med Sci Sports Exerc. 2020; 52: 278-286
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 * PubMed
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 * Google Scholar

,
81
 * Lee K
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 * Dieli-Conwright CM.

Effect of high-intensity interval training on patient-reported outcomes and
physical function in women with breast cancer receiving anthracycline-based
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84
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Adding high-intensity interval training to conventional training modalities:
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85
 * Mijwel S
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High-intensity exercise during chemotherapy induces beneficial effects 12 months
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86
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Physical deterioration and adaptive recovery in physically inactive breast
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,
88
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Effect of exercise on depression and fatigue in breast cancer women undergoing
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91
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Effect of low-intensity physical activity and moderate- to high-intensity
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101
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Effects of Tai Chi exercise on cancer-related fatigue in patients with
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The challenge of preserving cardiorespiratory fitness in physically inactive
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as well as yoga or light martial arts. Supplemental Table B.1 shows in detail
the intervention performed in each study. Intervention duration ranged from 3 to
27 weeks, while follow-up of outcome variables ranged from 3 weeks to 4 years
post-intervention. Thirty studies presented only immediate post-intervention
assessment data,
55
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RESULTS OF THE METHODOLOGICAL QUALITY AND RISK OF BIAS

Methodological quality was good in 27 (57.4%) of the 47 included studies
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Effect of a multimodal high intensity exercise intervention in cancer patients
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56
 * Alibhai SMH
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A phase II exercise randomized controlled trial for patients with acute myeloid
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59
 * Bolam KA
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Two-year follow-up of the OptiTrain randomised controlled exercise trial.
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60
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The effects of exercise on patient-reported outcomes and performance-based
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exercise and quality of life in acute leukemia (EQUAL).
Integr Cancer Ther. 2018; 17: 263-270
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61
 * Carayol M
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Short- and long-term impact of adapted physical activity and diet counseling
during adjuvant breast cancer therapy: the “APAD1” randomized controlled trial.
BMC Cancer. 2019; 19: 737-757
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68
 * Courneya KS
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Effects of aerobic and resistance exercise in breast cancer patients receiving
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J Clin Oncol. 2007; 25: 4396-4404
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69
 * Courneya KS
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Effects of exercise dose and type during breast cancer chemotherapy: multicenter
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J Natl Cancer Inst. 2013; 105: 1821-1832
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70
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Does exercise intensity matter for fatigue during (neo-)adjuvant cancer
treatment? The Phys-Can randomized clinical trial.
Scand J Med Sci Sports. 2021; 31: 1144-1159
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, 
71
 * Dhruva A
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77
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Effects of scheduled exercise on cancer-related fatigue in women with early
breast cancer.
ScientificWorldJournal. 2014; (2014)
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,
81
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Effect of high-intensity interval training on patient-reported outcomes and
physical function in women with breast cancer receiving anthracycline-based
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Support Care Cancer. 2021; 29: 6863-6870
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 * Scopus (7)
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,
84
 * Mijwel S
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 * et al.

Adding high-intensity interval training to conventional training modalities:
optimizing health-related outcomes during chemotherapy for breast cancer: the
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Breast Cancer Res Treat. 2018; 168: 79-93
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 * Google Scholar

, 
85
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High-intensity exercise during chemotherapy induces beneficial effects 12 months
into breast cancer survivorship.
J Cancer Surviv. 2019; 13: 244-256
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 * PubMed
 * Scopus (47)
 * Google Scholar

, 
86
 * Møller T
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Physical deterioration and adaptive recovery in physically inactive breast
cancer patients during adjuvant chemotherapy: a randomised controlled trial.
Sci Rep. 2020; 10: 1-15
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 * Scopus (19)
 * Google Scholar

,
88
 * Mostafaei F
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 * Salari N
 * Abbasi P.

Effect of exercise on depression and fatigue in breast cancer women undergoing
chemotherapy: a randomized controlled trial.
Heliyon. 2021; 7: e07657
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89
 * Naraphong W
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Exercise intervention for fatigue-related symptoms in Thai women with breast
cancer: a pilot study.
Nurs Health Sci. 2015; 17: 33-41
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, 
90
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Effectiveness of exercise-based rehabilitation on functional capacity and
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91
 * Travier N
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Effects of an 18-week exercise programme started early during breast cancer
treatment: a randomised controlled trial.
BMC Med. 2015; 13: 121-132
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, 
92
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Effects of an exercise program in colon cancer patients undergoing chemotherapy.
Med Sci Sports Exerc. 2016; 48: 767-775
 * Crossref
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,
94
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Effect of low-intensity physical activity and moderate- to high-intensity
physical exercise during adjuvant chemotherapy on physical fitness, fatigue, and
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J Clin Oncol. 2015; 33: 1918-1927
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,
95
 * Vincent F
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Home-based physical activity in patients with breast cancer: during and/or after
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Integr Cancer Ther. 2020; 191534735420969818
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97
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A randomized controlled trial of qigong on fatigue and sleep quality for
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Eur J Oncol Nurs. 2016; 23: 81-86
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98
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Tai Chi exercise for cancer-related fatigue in patients with lung cancer
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99
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Effects of nurse-led home-based exercise & cognitive behavioral therapy on
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100
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Effects of Tai Chi exercise on cancer-related fatigue in patients with
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J Pain Symptom Manage. 2018; 55: 737-744
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and fair in the remaining 20 (42.6%) studies
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Effects of exercise on biobehavioral outcomes of fatigue during cancer
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The effects of a six-week supervised multimodal exercise intervention during
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Effects of a walking intervention on fatigue-related experiences of hospitalized
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A nurse facilitated mind-body interactive exercise (Chan-Chuang qigong) improves
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 * View Large Image
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 * Download Hi-res image
 * Download (PPT)


CANCER-RELATED FATIGUE NETWORK META-ANALYSIS

Forty-two studies were included in the short-term network meta-analysis for a
total of 18 exercise interventions and 58 comparisons.
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76
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(fig 2). Supplemental Table A.5 shows the distribution of direct comparisons in
the included studies.
Fig 2Network graph. The network graph represents the comparisons (each
connection) between exercise modalities (nodes) that have been studied in the
different primary studies (or direct evidence). The thickness of the connection
between the different interventions represents the number of studies in data
specific comparison. Flexib, flexibility training.
 * View Large Image
 * Figure Viewer
 * Download Hi-res image
 * Download (PPT)

There was a trend that adding aerobic and resistance exercise (low-intensity)
(SMD=1.28, 95% CI -0.18; 2.75, P=.086) or aerobic and resistance exercise
(moderate-intensity) (SMD=0.85; 95% CI -0.12; 1.82, P=.087) was more effective
than adding flexibility training to UC. There were also favorable trends for
adding aerobic and resistance exercise (moderate-intensity) (SMD=-0.47, 95% CI
-0.96, 0.02, P=.060) vs UC alone (figs 3 and 4). No statistically significant
differences were found when comparing the addition of an exercise-based
intervention to UC vs UC alone. The interventions with the highest P-scores were
aerobic and/or resistance exercise of low- to moderate-intensity, with values
ranging from 0.835 to 0.702 (Supplemental Figs A.6 and A.7). Supplemental Fig
A.8 showed the orientation of the primary studies by means of a forest plot
without summary effect. The strength of the certainty was low to very low
(Supplemental Appendix A.2). Egger test for publication bias was not
statistically significant (P=.391) (Supplemental Fig A.9).
Fig 3Estimation of the effects from the network meta-analysis. Data are shown as
row treatments versus column treatments. Yellow boxes: tendency to statistical
significancy (P<0.1). Flexib, flexibility training.
 * View Large Image
 * Figure Viewer
 * Download Hi-res image
 * Download (PPT)

Fig 4Effect table with all network meta-analysis estimates. The effect size of
the comparisons has been represented in a color matrix. The number indicates the
pooled effect size based on direct and indirect evidence and the color ranges
between green (fatigue improves), yellow (no effect), and red (fatigue worsens).
Flexib, flexibility training.
 * View Large Image
 * Figure Viewer
 * Download Hi-res image
 * Download (PPT)

Supplemental Fig A.10 shows the direct and indirect evidence contribution
matrix. The information on direct and indirect comparisons is shown in
Supplemental Table B.2. The results of the net heat plot and splitting analysis,
which provides a detailed assessment of the inconsistency, are shown in
Supplemental Figs A.11 and A.12. There was no significant inconsistency in the
random-effects model.


FOLLOW-UP DATA

In the follow-up period (3 weeks to 4 years), most of the studies found no
significant differences on CRF between exercise intervention (adding low-,
moderate-, or high-intensity aerobic, resistance, and/or flexibility training or
yoga) and UC alone in patients with acute myeloid leukemia, breast or colon
cancer.
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94
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Effect of low-intensity physical activity and moderate- to high-intensity
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The few studies that showed significant differences in favor of adding exercise
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DISCUSSION

The aim of this systematic review and network meta-analysis was to compare the
effectiveness of different exercise modalities in decreasing CRF in patients
with cancer undergoing chemotherapy. Our results showed a positive trend in
favor of aerobic and/or resistance exercise (ie, moderate- or low-intensity)
over UC alone or UC with flexibility exercise, but the results were not
statistically significant.
Brownstein et al investigated physiological and psychosocial correlates of CRF
in cancer survivors. They found that peak oxygen consumption, maximal voluntary
contraction force, pain intensity, and pain severity were associated with CRF
severity.
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That is, CRF correlates with measures of functional capacity which improve with
the addition of exercise. Given our results, it is therefore necessary to
reconsider the implementation of exercise in patients with cancer undergoing
chemotherapy to understand the reason for the lack of effectiveness of exercise
to improve the experience of CRF. The current application of exercise in these
patients may not be optimal for managing CRF.
One limitation that may have influenced the results is the heterogeneity in the
implementation of exercise training. In the exercise groups, despite the
categorization of exercise modality and intensity, there were small differences
in terms of additional procedures (eg, nutritional or health advice) and/or
differences in the design or duration of exercise protocols. In the UC only
groups, there were slight differences in activities recommendations (eg,
suggestions to maintain, increase, or restrict physical activity).
Some barriers to exercise in the oncology population may limit the effectiveness
of exercise on CRF: low motivation, kinesiophobia, lack of social support, and
limited guidance by professionals about exercise.
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Patients have erroneous beliefs and lack of knowledge about CRF and exercise.
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It is possible that the way in which exercise is being implemented in patients
with cancer may not be optimal, and even counterproductive, to manage CRF.
Patients tend to continually worry about CRF. They perceive exercise as a CRF
trigger and rest as a reliever.
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Thus, patients are prone to physical inactivity, and exercise only during the
supervised training session. This behavior would result in the absence of
perceived benefit from the intervention by the patient, physical deconditioning
consequences, and the non-adherence to exercise over time. Appropriate
professionals should encourage a modification of patients’ behaviors and
beliefs. It is important that patients understand the concept of CRF, its
etiology, the influencing factors. We should consider that similar to the
application of exercise to manage pain in the pain patient,
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the management of CRF through exercise in the oncology patient should be
implemented through a conceptual approach that takes into account the patient's
conceptualization of CRF, the patient's expectations, the patient's exercise
experience, and the patient's fears about physical activity, among others.
There are multiple factors that can influence CRF and its experience by the
patient, making it a symptom highly dependent on the individuality of each
patient.
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Bower et al identified in patients with breast cancer that CRF could present
different trajectories, in terms of severity and persistence, from diagnosis to
survival. They also found associations between the presentation of CRF and
factors such as level of education, stage of disease, or psychosocial factors
(eg, depression, distress), confirming individual variability.
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The individual variability of CRF and the subjective nature of its assessment
may also affect the results derived from pooling and may not have been
representative of the individual patient data. We should consider the
individuality of CRF experience when implementing exercise programs.
Patients with breast cancer experienced CRF onset even before the start of
chemotherapy. These symptoms were worse at the end of treatment and tended to
return to baseline values only after chemotherapy.
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It may be interesting to initiate the exercise interventions before the start of
chemotherapy. Exercise as prehabilitation could prepare the patient to cope with
treatment adverse effects and improve its effectiveness.
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Inadequate diagnosis limits patients' access to interventions to reduce CRF.
There is also considerable variability in the instruments (and CRF dimensions)
used to assess CRF. Differences in the characteristics and dimensions of CRF
instruments could have biased the results. This specific concern may be 1 of the
causes of the poor exercise effectiveness found in our review. Actually, results
from a dyspnea-based study lead us in this direction: Wadell et al found that
chronic respiratory patients improved on the affective and effect dimensions of
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If CRF assessment were standardized and more specifically assessed, we could
analyze the effectiveness of exercise interventions on each of the CRF
dimensions.
Our findings showed that exercise modality seems to be a factor to consider when
employing exercise in combination with first-choice treatment in patients with
cancer. Aerobic and/or resistance exercise was effective in reducing CRF.
Regarding exercise intensity, there were favorable results with low- or
moderat-intensity. Most of favorable results were at low- to moderate-intensity,
coinciding with the highest P-scores. Future studies are needed to evaluate
whether high-intensity exercise training may be less effective in CRF solely
because of the perceived threatening situation and lack of confidence felt by
the patient, or because low- to moderate-intensity is sufficient.
The multifactorial mechanisms of CRF remain to be elucidated. It involves
alterations at the biochemical, physiological and/or psychological levels, among
others.
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Three types of factors have been reported to capture the physiological and
psychological processes involved in CRF: (1) predisposing factors—patient's
characteristics that increase the risk of developing CRF (eg, age, genetics,
anxiety, depression), (2) precipitating factors—contexts that trigger the onset
of CRF (eg, sudden change in cancer severity or treatment), and (3) perpetuating
factors—behaviors that worsen or facilitate CRF chronification (eg, physical
inactivity, inadequate diet, and sleep).
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This could, at least in part, explain the paucity of results. It is possible
that multimodal interventions (including, for example, psychological, dietary,
or behavioral-sleep counselling) that address modifiable factor may be more
effective in preventing and mitigating CRF.
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Regarding the follow-up period, most studies did not show statistically
significant differences between groups. It highlights the likely inadequacy of
exercise implementation in these patients. Failure to modify patients' beliefs
and behaviors in relation to exercise would impede the long-term adherence. At
the end of the exercise intervention and the study period, patients do not
maintain exercise and return to physical inactivity. Some studies did present
significant differences in some of CRF dimensions at follow-up (eg, cognitive or
emotional CRF). As commented previously, a better assessment of the CRF could
lead to different results according to the dimensions.


STUDY LIMITATIONS

This systematic review with network meta-analysis had some limitations that
should be acknowledged. First, an inherent limitation of network meta-analysis
design is that it leads to a certain degree of imprecision. Imprecision and
indirect evidence have been taken in consideration when determining the strength
of evidence (ie, low to very low, according to the GRADE). The results should be
interpreted with caution because of the large amount of indirect evidence. We
need more direct comparisons to provide more robust conclusions on the effects
of exercise in reducing CRF. Second, we must consider the variability between
studies in terms of cancer type and stage, chemotherapy treatments, as well as
heterogeneity in exercise protocols. Third, to perform the network meta-analysis
we grouped and categorized the exercise according to modality and intensity.
Regarding modality, there may be some differences between interventions within
the same category (eg, light martial arts). Some interventions were multimodal
and included, for example, nutrition or recommendations. This could not be
considered as they were not interventions quantified in the studies. Other
classifications may lead to differences in the results. Fourth, CRF is a patient
self-reported variable, which may introduce some level of bias in the results.
In addition, there was great variability in the type of scale used and the
assessed dimensions. We should consider the lack of standardization in this
regard. Fifth, the methodological quality was fair in almost half of the studies
and all of them had an assessment ranging from some concerns to high risk of
bias. Sixth, it should be noted that the analysis included pilot studies (1
study of 5 with moderate-intensity resistance exercise, 2 studies of 6 with
moderate-intensity aerobic exercise, 1 study of 6 with moderate-intensity
aerobic and resistance exercise, and 1 study of 3 with yoga). However, they
represent only a small proportion of the included studies (5 of 47 studies,
10.6%). Seventh, most of the comparisons between the different exercise
modalities (not with only usual care) were calculated with indirect evidence.
Future studies should begin to compare the addition of different exercise
modalities rather than just comparing the addition of an exercise modality with
no addition. The reader should be aware that effect sizes calculated totally or
partially from indirect evidence are inferred and do not accurately represent
reality. Thus, we should interpret them cautiously. Eighth, we included a large
amount of exercise modalities for a large number of comparisons (18 exercise
modalities and 58 comparisons) which may have led to multiplicity issues.
Finally, we were unable to statistically synthesize the follow-up data, because
of the small number of articles that reported it.


CONCLUSIONS

The addition of low- to moderate-intensity aerobic and/or resistance exercise
showed positive trends compared to UC alone or UC in combination with
flexibility training, although the differences were not significant. In light of
the overall benefits of exercise in these patients, a reconceptualization of how
exercise modalities are implemented in patients with cancer undergoing
chemotherapy is required to better adapt to the multifactorial characteristics
of CRF. Heterogeneity and lack of standardization of CRF assessment need to be
considered for the design of future clinical studies.


APPENDIX. SUPPLEMENTARY MATERIALS

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ARTICLE INFO


PUBLICATION HISTORY

Published online: January 31, 2023
Accepted: January 11, 2023
Received in revised form: January 8, 2023
Received: July 8, 2022


PUBLICATION STAGE

In Press Journal Pre-Proof


FOOTNOTES

Study registration: PROSPERO, CRD42022292706.

Disclosures: none.


IDENTIFICATION

DOI: https://doi.org/10.1016/j.apmr.2023.01.008


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SCIENCEDIRECT

Access this article on ScienceDirect
Effectiveness of Therapeutic Exercise Models on Cancer-Related Fatigue in
Patients With Cancer Undergoing Chemotherapy: A Systematic Review and Network
Meta-analysis
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FIGURES

 * Fig 1Risk of bias assessment: (A) summary for individual studies and (B)
   aggregate appraisal results.
 * Fig 2Network graph. The network graph represents the comparisons (each
   connection) between exercise modalities (nodes) that have been studied in the
   different primary studies (or direct evidence). The thickness of the
   connection between the different interventions represents the number of
   studies in data specific comparison. Flexib, flexibility training.
 * Fig 3Estimation of the effects from the network meta-analysis. Data are shown
   as row treatments versus column treatments. Yellow boxes: tendency to
   statistical significancy (P<0.1). Flexib, flexibility training.
 * Fig 4Effect table with all network meta-analysis estimates. The effect size
   of the comparisons has been represented in a color matrix. The number
   indicates the pooled effect size based on direct and indirect evidence and
   the color ranges between green (fatigue improves), yellow (no effect), and
   red (fatigue worsens). Flexib, flexibility training.




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