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Authors:

Deborah Tomlinson, MN, RN


Caroline Diorio, HBSc Cancer
Joseph Beyene, PhD
Lillian Sung, MD, PhD

Affiliations:
From the Child Health Evaluative ORIGINAL RESEARCH ARTICLE
Sciences (DT, CD, LS) and the Division
of Haematology/Oncology (LS), The
Hospital for Sick Children, Toronto,
Ontario, Canada; and the Department
of Clinical Epidemiology and Effect of Exercise on
Biostatistics (JB), McMaster University,
Hamilton, Ontario, Canada. Cancer-Related Fatigue
Correspondence: A Meta-analysis
All correspondence and requests for
reprints should be addressed to: Lillian
Sung, MD, PhD, Division of
Haematology/Oncology, The Hospital ABSTRACT
for Sick Children, Toronto, Ontario, Tomlinson D, Diorio C, Beyene J, Sung L: Effect of exercise on cancer<related
Canada, M5G 1X8.
fatigue: a meta-analysis. Am J Phys Med Rehabil 2014;93:675Y686.
Disclosures: Numerous randomized controlled trials have been conducted to determine efficacy
Deborah Tomlinson and Caroline of exercise on cancer-related fatigue. However, many trials lacked sufficient power
Diorio contributed equally to demonstrate significant differences, and little is known about how the effect
to this study.
Financial disclosure statements have of exercise differs depending on patient- and intervention-level characteristics.
been obtained, and no conflicts of A meta-analysis was performed to determine whether exercise reduces fatigue
interest have been reported by the compared with usual care or nonexercise control intervention in patients with can-
authors or by any individuals in control
of the content of this article. cer. The authors searched Ovid MEDLINE, EMBASE, PsycINFO, The Cochrane
Central Register of Controlled Trials, and CINAHL. Two authors independently
Editor’s Note: extracted the data. Randomized controlled trials comparing exercise with control
Supplemental digital content is intervention in cancer patients in which fatigue was quantified were eligible. Seventy-
available for this article. Direct URL two randomized controlled trials were identified, 71 in adults and 1 in children. Exer-
citations appear in the printed text and
cise had a moderate effect on reducing fatigue compared with control intervention.
are provided in the HTML and PDF
versions of this article on the journal_s Exercise also improved depression and sleep disturbance. Type of exercise did not
Web site (www.ajpmr.com). significantly influence the effect on fatigue, depression, or sleep disturbance. Exer-
0894-9115/14/9308-0675 cise effect was larger in the studies published 2009 or later. There was only one
American Journal of Physical pediatric study. The results of this study suggest that exercise is effective for the
Medicine & Rehabilitation management of cancer-related fatigue.
Copyright * 2014 by Lippincott
Williams & Wilkins Key Words: Fatigue, Depression, Sleep Disturbance, Aerobic Exercise, Walking, Yoga

DOI: 10.1097/PHM.0000000000000083

www.ajpmr.com Exercise is Effective for the Management of CRF 675

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
F atigue has been increasingly recognized as an
important symptom during and after treatment of
used a combination of medical subject headings and
text words including fatigue, neoplasm, and exercise
therapy, and studies were limited to RCTs. Appendix 1
cancer, impacting on physical, mental, and emo- (http://links.lww.com/PHM/A70) illustrates the com-
tional functioning. Fatigue may be characterized by plete search strategy.
a lack of energy, decreased physical ability, and
feelings of tiredness.1Y3 Cancer-related fatigue Study Selection
(CRF) has been described as an unexpected tired-
For this review, similar to that of Hayden et al.,25
ness that is more intense and more severe than
the authors considered the following as forms of exer-
normal fatigue,4,5 which is not relieved by sleep or rest.
cise: (1) aerobic exercise, (2) resistance exercise/muscle
Up to 80%Y90% of patients treated with radiation or
strengthening, (3) walking, (4) pilates, (5) yoga, (6)
chemotherapy experience CRF.6 Fatigue rarely oc-
stretching exercises aimed at increasing the amount
curs in isolation, and it is usually correlated with
of movement of joints or series of joints, and (7) other
other symptoms, particularly depression and sleep
(including unspecified and tai chi). If a study included
disturbance.7Y11 Guidelines from the National Com-
multiple forms of exercise in the intervention arm,
prehensive Cancer Network recommend that the
categorization was conducted hierarchically in the
management of fatigue should be included in
order presented.
institutional quality improvement initiatives.12
The inclusion and exclusion criteria were de-
Many interventions have been evaluated to de-
fined a priori. The authors included studies in
termine their efficacy to prevent or treat CRF.13Y20 In
which (1) patients were randomly assigned to an
particular, exercise may be an effective intervention.21Y23
exercise intervention and a control intervention
Numerous randomized controlled trials (RCTs) have
(usual care or a nonexercise intervention), (2) pa-
been conducted to determine whether exercise can
tients were diagnosed with cancer and were in ac-
reduce fatigue. However, many of these trials had small
tive treatment or follow-up, and (3) fatigue was a
sample sizes and had insufficient power to demon-
primary or secondary outcome. Exclusion criteria
strate significant differences in fatigue. Furthermore,
were applied in a hierarchical fashion as follows:
little is known about how the effect of exercise dif-
(1) allocation was not randomly assigned, (2) treat-
fers depending on patient- and intervention-level
ment arm was not one of the identified exercised
characteristics.
interventions, (3) no control arm or control arm was
The authors hypothesized that, by synthesiz-
one of the identified exercise interventions, (4) study
ing all available RCTs, they would be able to improve
participants had not been diagnosed with cancer,
their precision in the measurement of an exercise
(5) fatigue was not reported to be quantified, (6)
treatment effect for fatigue. Furthermore, the au-
publication was a duplicate, (7) publication was not
thors hypothesized that they may also be able to ex-
in English, and (8) publication was a conference
plain heterogeneity in treatment effect by using a
proceeding or thesis.
meta-analytic approach. Consequently, the primary
Two reviewers (D. Tomlinson and C. Diorio)
objective was to determine whether exercise reduces
independently evaluated the titles and abstracts
fatigue compared with usual care or a nonexercise
identified by the search strategy, and potentially
control intervention in patients with cancer. The sec-
relevant publications were retrieved in full. The
ondary objective was to determine whether exercise
reviewers were not blinded to study authors or
reduces depression or sleep disturbance more than
outcomes. Final inclusion of studies into the meta-
control intervention does.
analysis was determined by agreement between
both reviewers. Agreement was evaluated using
METHODS the kappa statistic. Strength of agreement was de-
Data Sources and Searches fined as slight (0.00Y0.20), fair (0.21Y0.40), moderate
(0.41Y0.60), substantial (0.61Y0.80), or almost per-
Standard guidelines were followed for the con-
fect (0.81Y1.00).26
duct and reporting of this meta-analysis.24 Electronic
searches of the following databases were performed:
Ovid MEDLINE (1948 to May 2012), EMBASE (1980 Data Extraction and Quality Assessment
to May 2012), PsycINFO (1806 to June 2012), The Two reviewers (D. Tomlinson and C. Diorio)
Cochrane Central Register of Controlled Trials abstracted all data independently; case report forms
(Evidence Based Medicine Reviews, until May 2012), were reviewed, and discrepancies were resolved by
and CINAHL (1981 to June 2012). The search strategy consensus. The primary outcome measure was the

676 Tomlinson et al. Am. J. Phys. Med. Rehabil. & Vol. 93, No. 8, August 2014

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
fatigue score at the end of the intervention or Measures with opposite scaling were harmonized
the closest follow-up time point after the end of by multiplying the measure by 1.29 SMD can be in-
intervention. Secondary outcomes were depres- terpreted as follows: 0.20 is a small effect, 0.50 is a
sion and sleep disturbance at the end of the inter- medium effect, and 0.80 is a large effect.30
vention period. Weighted mean differences (WMDs) were also
Study quality was assessed by the Jadad scale,27,28 calculated for the most commonly used scale for each
which examines adequacy of randomization, double outcome to facilitate clinical interpretation of the ex-
blinding, and description of withdrawals and drop- ercise effect. For the primary outcome of fatigue, the
outs. For the purpose of describing the included most commonly used scale was the Functional As-
studies, the authors present the summary Jadad sessment of Cancer TherapyYFatigue (FACT-F) in ten
scores (range, 0Y5), in which a higher score is asso- studies, whereas for the secondary outcomes, the
ciated with better quality. Agreement was measured most commonly used scales were the Centre for
in the assessment of the Jadad score using the qua- Epidemiologic StudiesYDepression for depression in
dratic weighted kappa statistic. eight studies and the European Organization for
For studies in which there were missing fatigue Research and Treatment of Cancer Quality of Life
data (n = 23), the corresponding author was con- Questionnaire Core 30Yinsomnia subscale for sleep
tacted to retrieve further information. Additional in- disturbance in ten studies.
formation was provided for eight studies. A random-effects model was used for analy-
ses31 because heterogeneity was anticipated be-
Data Synthesis and Analysis tween studies. To explore sources of heterogeneity,
This meta-analysis combined data at the study stratified analyses were conducted by the follow-
level and not at the individual patient level. All ing variables: (1) exercise type, (2) sex, (3) delivery
synthesized outcomes were continuous in nature. type (home-based vs. supervised), (4) cancer treat-
The following assumptions were made to allow data ment status (on vs. off treatment), and (5) under-
synthesis: the mean can be approximated by the me- lying cancer diagnosis (hematologic malignancy
dian, and the interquartile range contains 1.35 SD.29 vs. solid tumor vs. mixed diagnoses). Subgroups
Many different measures were used for the pri- were included if there were at least two studies
mary and secondary outcomes. There were 15 sepa- within a stratum.
rate measures for fatigue, 5 separate measures for Publication bias occurs when small studies are
depression, and 4 separate measures for sleep dis- differentially published only if the results are posi-
turbance. Consequently, the main analytic approach tive. Publication bias was identified by depicting a
evaluated the standardized mean difference (SMD). funnel plot, which is a graph with the effect size

FIGURE 1 Flow diagram of trial identification and selection.

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Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
(SMD) on the x-axis and the inverse of variance of reviews, articles, and targeted journals. Seventy-two
the effect on the y-axis. Asymmetry, without studies studies were included.10,34Y104 There was substantial
in the bottom left or right corner depending on the agreement between the two reviewers on articles for
effect measure, suggests publication bias.32 In the inclusion with a J statistic of 0.72 (95% confidence
event that publication bias was suggested, the Btrim interval [CI], 0.56Y0.88). Characteristics of the in-
and fill[ technique was used to determine the impact cluded studies are summarized in Table 1 and detailed
of such bias.32 This technique involves deleting out- in Appendix 2 (http://links.lww.com/PHM/A70). There
lying studies and creating hypothetical negative stud- was considerable variability in the following: partic-
ies with equal weight to determine the robustness of ipant characteristics; type, intensity, and duration of
the conclusions of the analysis. intervention; length of time of the exercise sessions; and
This meta-analysis was performed using Review the outcome measures used. Overall, the 72 studies
Manager (RevMan; version 5.1; The Cochrane Collab- included 5367 participants, of whom 2740 were
oration, Oxford, United Kingdom). All tests of signifi- randomized to exercise and 2627 were randomized to
cance were two sided, and statistical significance was control intervention. Seventy-one studies were con-
defined as P G 0.05. ducted in adults, and one study was conducted in
children.72 The median Jadad score for study quality
Role of the Funding Source was 2 (range, 0Y5). Agreement in study quality score
The funding source had no role in the design, determination was moderate (J = 0.58; 95% CI,
conduct, or reporting of this analysis or in the de- 0.44Y0.72).
cision to submit the manuscript for publication. Table 2 and Figure 2 demonstrate that exercise
has a moderate effect on reducing fatigue compared
with control intervention (SMD, j0.45; 95% CI, j0.57
RESULTS to j0.32; n = 56 studies; P G 0.001). The most com-
Figure 1 illustrates the flow diagram of trial mon fatigue measure used was the FACT-F, and
identification and selection based on the Preferred among the studies that used this instrument, exercise
Reporting Items for Systematic Reviews and Meta- significantly reduced fatigue (WMD, j2.55; 95% CI,
Analyses (PRISMA) template.33 An additional 11 studies j4.13 to j0.98; n = 10 studies; P = 0.002). Table 2 and
were identified through hand searches of other Appendix 3a and 3b (http://links.lww.com/PHM/A70)
illustrate that exercise also had a moderate effect on
reducing depression and sleep disturbance.
TABLE 1 Characteristics of included studies of Table 3 illustrates the results of the stratified
exercise to reduce fatigue in patients analysis for the primary outcome of fatigue. The
with cancer (N = 72) benefit of exercise did not differ by type of exercise
Characteristic Studies, n (%) intervention (P for interaction = 0.85). However,
the effect of exercise on fatigue reduction may differ
Sex
Male 7 (9.7) by underlying malignancy type, with a stronger ef-
Female 33 (45.8) fect in solid tumor vs. hematologic and mixed ma-
Both 32 (44.4) lignancy types (P for interaction = 0.01). None of
Exercise type
Aerobic 14 (19.4)
the other stratification variables including on or off
Walking 19 (26.4) treatment status influenced the exercise effect.
Yoga 9 (12.5) Appendix 4a (http://links.lww.com/PHM/A70)
Resistance 3 (4.2) illustrates the stratified analysis for the secondary
Mixed 22 (30.6)
Othera 5 (6.9) outcome of depression. In the evaluation of exercise
Delivery method type, resistance was excluded because there were
Home based 26 (36.1) fewer than two studies in that stratum. The effect of
Supervised 46 (63.9)
Treatment status exercise on improving depression did not differ by
On treatment 24 (33.3) type of exercise (P for interaction = 0.07). However,
Off treatment 46 (63.9) the effect of exercise on depression may differ by
Both 2 (2.8)
Malignancy type
sex, with a stronger effect in females compared with
Hematologic 8 (11.1) males (P for interaction = 0.03).
Mixed 45 (63.9) The stratified analysis for sleep disturbance is illus-
Solid tumor 19 (26.4) trated in Appendix 4b (http://links.lww.com/PHM/A70).
a
Other includes exercise not specified and tai chi. Sex was not evaluated because only one study was
available in the Bmale[ stratum. For the stratified

678 Tomlinson et al. Am. J. Phys. Med. Rehabil. & Vol. 93, No. 8, August 2014

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
TABLE 2 Summary of outcomes of exercise vs. control interventions
Range No. No. Effect Estimatea
Outcome Scores Studies Participants (95% CI) I2, % P
Fatigue
All studies, SMD 56 4000 j0.45 (j0.57 to j0.32) 71 G0.001
FACT-F, WMD 0 to 52 10 794 j2.55 (j4.13 to j0.98) 27 0.002
Depression
All studies, SMD 20 1658 j0.41 (j0.63 to j0.19) 71 G0.001
CES-D, WMD 0 to 60 8 654 j0.53 (j1.32 to 0.26) 0 0.19
Sleep disturbance
All studies, SMD 17 1125 j0.27 (j0.43 to j0.12) 32 G0.001
EORTC-QLQ-C30-Insomnia, WMD 0 to 100 10 788 j7.83 (j11.76 to j3.90) 0 G0.001
a
All analyses used a random-effects model.
CES-D, Centre for Epidemiologic StudiesYDepression; EORTC-QLQ-C30-Insomnia, European Organization for Research and
Treatment of Cancer Quality of Life Questionnaire Core 30Yinsomnia subscale.

FIGURE 2 Forest plot of fatigue reduction after an exercise vs. control intervention for patients with cancer.

www.ajpmr.com Exercise is Effective for the Management of CRF 679

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TABLE 3 Stratified analysis of the effect of exercise on fatigue
Outcome/Subgroup No. Studies No. Participants Effect (95% CI)a I2 , % P for Interaction
Sex 30 2109
Female 24 1684 j0.61 (j0.85 to j0.37) 81 0.81
Male 6 425 j0.55 (j0.93 to j0.18) 68
Exercise type 52 3855 0.85
Aerobic 14 3855 j0.43 (j0.80 to j0.06) 85
Walking 11 890 j0.37 (j0.58 to j0.15) 58
Yoga 7 889 j0.40 (j0.72 to j0.07) 56
Resistance 2 322 j0.49 (j1.41 to 0.44) 68
Mixed 18 1475 j0.52 (j0.69 to j0.35) 54
Delivery method 56 4000 0.21
Home based 19 1399 j0.33 (j0.58 to j0.08) 80
Supervised 37 2601 j0.51 (j0.65 to j0.37) 62
Treatment status 56 4000 0.13
On treatment 34 2618 j0.38 (j0.51 to j0.24) 62
Off treatment 20 1222 j0.61 (j0.88 to j0.33) 79
Mixed 2 160 j0.18 (j0.49 to 0.13) 0
Malignancy type 56 4000 0.01
Hematologic 8 484 j0.33 (j0.51 to j0.15) 0
Solid 34 2298 j0.60 (j0.80 to j0.41) 79
Mixed 14 1218 j0.22 (j0.39 to j0.05) 48
a
All analyses used a random-effects model.

analysis of exercise type, walking and resistance were j0.43; P G 0.001 in studies published 2009 or later
excluded because there were fewer than two studies (P for interaction = 0.003).
in these strata. The type of exercise did not influence
the benefit of exercise on sleep disturbance (P for DISCUSSION
interaction = 0.53). No significant interactions were In this meta-analysis that included 5367 par-
noted in this analysis. ticipants, the authors found that exercise had a mod-
Appendices 5a, 5b, and 5c illustrate the funnel erate effect in reducing fatigue, depression, and sleep
plots for fatigue, depression, and sleep disturbance. disturbance. Given the interrelationship between
Publication bias was suggested for fatigue and de- these three symptoms, it is not surprising that effects
pression, with one outlying study by Kim et al.76 were similar across all outcomes. The large number of
For fatigue, when this one study was removed and studies and the consistency in effect suggest that ex-
when a hypothetical negative study of equal weight ercise is effective in reducing these symptoms.
was added, the interpretation did not change sub- Although the effect size for fatigue reduction was
stantively (SMD, j0.40; 95% CI, j0.51 to j0.29; moderate, some may question whether the reduction
P G 0.001, and SMD, j0.41; 95% CI, j0.56 to j0.27; in WMD according to the FACT-F of 2.55 is clinically
P G 0.001, respectively). Similar findings were seen meaningful. Cella et al.105 (2002) found that a differ-
with depression (SMD, j0.25; 95% CI, j0.37 to ence in FACT-F score of 3 was a clinically important
j0.13; P G 0.001, and SMD, j0.28; 95% CI, j0.58 difference. Santana et al.106 reported a mean differ-
to 0.03; P = 0.07, respectively). ence of 5.0 (SE, 1.06) in cancer patients who rated
It was noted that in the forest plot of exercise fatigue as worse and a mean difference of 1.28 (SE,
ordered by year of publication, the effect seemed 1.00) in those who reported fatigue as the same.
to change over time. Thus, a post hoc analysis These studies suggest that a difference of 2.55 for
was conducted in which the effect of exercise was the FACT-F may be important to patients.
stratified by year of publication. The median year Two pertinent negative tests for interaction
of publication (2009) was selected as the cutoff were a lack of difference in exercise effect according
for stratification (G2009 vs. Q2009) (Appendix 6 to exercise type and patient treatment status (on vs.
[http://links.lww.com/PHM/A70]). This analysis illustrated off treatment for cancer). The former suggests that
that the effect of exercise is larger in studies pub- all types of exercise may be encouraged for fatigue
lished more recently, with SMD of j0.25; 95% reduction. The latter suggests that future meta-
CI, j0.40 to j0.10; P = 0.001, in studies published analyses may consider combining these patient types.
before 2009 and SMD of j0.61; 95% CI, j0.79 to There were also two important subgroup differences

680 Tomlinson et al. Am. J. Phys. Med. Rehabil. & Vol. 93, No. 8, August 2014

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
that emerged. The effect of exercise on fatigue seemed less, this result must be interpreted very cautiously
to differ by disease group, with patients with solid tu- because this analysis was not planned a priori and
mors benefiting the most from exercise. The authors thus is subject to type I error.
also found that the effect of exercise on depression In this review, the terms exercise and physical
seemed to differ by sex, with larger effect in women. activity were used interchangeably. Others have
This meta-analysis is complementary to two re- drawn a distinction between the two, with physical
cent meta-analyses of the effect of exercise on several activity being defined as any bodily movement that
domains of quality-of-life for adults who are cancer uses energy. Physical activity may be structured
survivors22 and who are receiving active anticancer or unstructured. Conversely, exercise is a subset of
treatment.23 These reviews included fatigue as one of physical activity in which activity is structured,
the domains evaluated. They also reported that exer- repetitive, and conducted with the goal of improv-
cise significantly reduces CRF at the 12-wk follow-up ing physical health.108,109 In this review, all of
for survivors (SMD, j0.82; 95% CI, j1.50 to j0.14)22 the studies that were included focused on exercise
and for those in therapy (SMD, j0.73; 95% CI, j1.14 rather than unstructured physical activity given that
to j0.31).23 There are several differences between all of the studies were randomized trials. However,
the approaches of these reviews and the approach of the authors do not know whether unstructured
this study. First, those two reviews included both physical activity may have an important role to play
RCTs and quasi-randomized controlled clinical trials. in terms of reduction in fatigue and improvement
It is possible that the inclusion of the latter led to in outcomes.
biased results because quasi randomization may result An important limitation of the literature is the
in nonconcealed allocation, and nonconcealed alloca- lack of clarity regarding what exercise means in
tion has been associated with exaggerated treatment terms of supervised exercise by physical therapists
effects.107 Second, those reviews included disserta- vs. supervised exercise by fitness professionals vs.
tions and conference abstracts. Although there is self-regulated exercise. Because the primary studies
considerable debate about the inclusion of these pub- did not articulate these issues well, it is not possible
lication types, given that they are not peer reviewed, to evaluate the efficacy of supervised exercise that
data quality may be inferior to peer-reviewed publi- is prescribed by rehabilitation professionals com-
cations. Finally, this review included an additional pared with other forms of exercise. It is important
15 studies that were not identified in those re- to emphasize that all exercise is not the same and
views37,38,44,45,68,70,72,73,76,78,79,89,92,103,104 because that these distinctions are important for primary
the focus of the reviews was slightly different. healthcare providers to consider in the prescription
Nonetheless, the consistent findings between these of exercise for patients with cancer. In addition, it
reviews despite different methodological approaches is important for future research to begin to disen-
strengthen the confidence in the findings. tangle the effects of these different modes of exercise
In a stratified analysis by exercise type, the delivery such that the optimal approach can be used
authors did not find that the type of exercise influ- for future patients.
enced the effect of exercise on fatigue. With a scarcity Current empirical evidence suggests a low in-
of literature on the mechanism or dose-response char- cidence of adverse events related to exercise in pa-
acteristics of exercise, this finding is important to tients with cancer. Although adverse events may be
clinical practice. Cancer patients, particularly those dependent on the characteristics of the cancer and
receiving more aggressive therapies, may be unable the type of treatment, most reported events are car-
or reluctant to undertake more strenuous aerobic diovascular.110 However, this literature is only re-
exercise. This analysis suggests that less intense ex- cently emerging, and safety issues with different
ercise such as yoga and stretching may be similarly modalities of exercise prescription have not been
effective and thus may be ideal for specific subsets of fully described.110,111 In recognition of this impor-
patients with CRF. tant issue, the American College of Sports Medicine
The authors performed a post hoc stratified anal- convened a panel to develop guidelines that address
ysis by year of publication and found that exercise had safety issues.112 The guidelines suggested that Bexer-
greater effect on fatigue in those studies published cise testing and prescription are best done by exercise
in 2009 or later. The reason for this finding is unclear. professionals or physical therapists in consultation
It is possible that exercise interventions have im- with the cancer care team.[112 It is important to em-
proved, thus increasing the effect size. However, it phasize that in the prescription of exercise to patients
is also possible that more recent studies are more who are actively undergoing treatment and who are
poorly designed with greater risk for bias. Nonethe- acutely ill, safety concerns must be a priority and

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