Beruflich Dokumente
Kultur Dokumente
Review
The NEIL Programme, Institute of Neuroscience, Trinity College Dublin, Dublin 2, Ireland
Department of Statistics, Trinity College Dublin, Dublin 2, Ireland
a r t i c l e
i n f o
Article history:
Received 7 January 2014
Received in revised form 8 May 2014
Accepted 13 May 2014
Available online 23 May 2014
Keywords:
Systematic review
Meta-analysis
Exercise
Physical activity
Cognitive functioning
Healthy older adults
a b s t r a c t
Data from epidemiological, cross-sectional, and neuroimaging research show a relationship between
higher levels of exercise and reduced risk of cognitive decline but evidence from randomised controlled
trials (RCTs) is less consistent. This review examines the impact of aerobic exercise, resistance training,
and Tai Chi on the cognitive function of older adults without known cognitive impairment. We investigate explanations for inconsistent results across trials and discrepancies between evidence from RCTs
and other research data. Twenty-ve RCTs were included in the review. Meta-analysis results revealed
signicant improvements for resistance training compared to stretching/toning on measures of reasoning (p < 0.005); and for Tai Chi compared to no exercise controls on measures of attention (p < 0.001) and
processing speed (p < 0.00001). There were no signicant differences between exercise and controls on
any of the remaining 26 comparisons. Results should be interpreted with caution however as differences
in participant proles, study design, exercise programmes, adherence rates, and outcome measures contribute to both discrepancies within the exercise research literature and inconsistent results across trials.
2014 Elsevier B.V. All rights reserved.
Contents
1.
2.
3.
4.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.
Search strategy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Selection criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.
Statistical analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1.
Included studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.
Aerobic exercise versus stretching/toning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.3.
Aerobic exercise versus no exercise active control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.4.
Aerobic exercise versus no intervention . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.5.
Resistance versus stretching/toning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.6.
Resistance versus no exercise active control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.7.
Tai Chi versus no exercise active control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.
Exercise-types . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.1.
Aerobic exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
13
13
13
14
14
14
14
14
14
22
23
24
24
25
28
28
Corresponding author at: The NEIL Programme, Institute of Neuroscience, Trinity College Dublin, The Alzheimer Society of Ireland, Room 3.10, Lloyd Building, Dublin 2,
Ireland. Tel.: +353 1 896 4505.
E-mail addresses: kellym50@tcd.ie (M.E. Kelly), loughred@tcd.ie (D. Loughrey), lawlorb@stjames.ie (B.A. Lawlor), iroberts@tcd.ie (I.H. Robertson), walshc@tcd.ie (C. Walsh),
brennas1@tcd.ie (S. Brennan).
http://dx.doi.org/10.1016/j.arr.2014.05.002
1568-1637/ 2014 Elsevier B.V. All rights reserved.
4.1.2.
Resistance training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.3.
Tai Chi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.
Discrepancies between RCT evidence and other exercise literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.1.
Baseline physical performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.2.
Length of intervention and follow-up . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.3.
Efciency of the intervention and adherence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.4.
Physical tness and cognitive health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.3.
Inconsistent results across RCTs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.4.
Limitations of the review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.5.
Conclusions and recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conicts of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Appendix A.
Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
As the incidence of age-related cognitive impairment increases,
there is an interest in explaining the role of physical activity in
improving cognitive function of older adults and delaying the onset
of cognitive decline. Although accumulating research evidence
from epidemiological, cross-sectional and neuroimaging studies
shows that exercise is benecial to cognitive health, evidence from
randomised controlled trials (RCTs) is less consistent. Further clarication is necessary to determine if exercise interventions truly
benet cognitive function, particularly for older adults who are at
a greater risk of cognitive decline.
Epidemiological research shows a consistent relationship
between higher levels of physical activity and reduced risk of cognitive decline and dementia. A meta-analysis of 16 prospective
studies examining the relationship between physical activity and
risk of neurodegenerative disease reported that engaging in the
highest physical activity category reduced the risk of dementia by
28% and Alzheimers Disease (AD) by 45%, compared to the lowest physical activity category, even after controlling for possible
confounding factors including age, education, vascular risk factors,
other medical conditions, and ApoE4 genotype (Hamer and Chida,
2009). In a more recent meta-analysis of 15 prospective cohort
studies, over thirty thousand healthy older adults were followed
for periods of 112 years. Results showed that individuals who
engaged in higher levels of physical activity at baseline had a 38%
reduced risk of cognitive decline at follow-up compared to those
who led a sedentary lifestyle at baseline (So et al., 2011).
Epidemiological evidence is supported by cross-sectional studies that show that older adults who reported greater engagement
in physical activity, compared to those who reported being inactive, had a reduced risk of cognitive impairment (e.g. Middleton
et al., 2010) and improved performance on a range of executive function tasks (see Guiney and Machado, 2013 for a review).
Cross-sectional studies using actigraphy as an objective measure of
exercise engagement reported that compared with elderly individuals in the lowest tertile of physical activity, those in the highest
tertile performed signicantly better on tests of global cognition and executive functioning (Barnes et al., 2008; Brown et al.,
2012). Neuroimaging research provides further supportive evidence, showing that compared to those who were less t or led
sedentary lifestyles, older adults with higher aerobic tness levels
had reduced rates of age-related atrophy of grey and white matter
(Colcombe et al., 2003), greater grey matter density in prefrontal
and temporal regions (Gordon et al., 2008), superior white matter
density in the corpus callosum (Johnson et al., 2012), and larger hippocampal volumes (Erickson et al., 2009). Despite the accumulating
evidence from epidemiological, cross-sectional, and neuroimaging
research on the benets of exercise for cognitive function, data from
RCTs is largely inconsistent.
13
28
28
28
28
28
28
29
29
29
30
30
30
30
30
14
exclude articles that did not meet inclusion criteria. Full texts
of remaining studies were then screened for eligibility by two
independent reviewers. Disagreements were resolved through
discussions with our expert authors (study selection owchart,
Appendix B).
2.2. Selection criteria
We followed PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines. Trials were included
that investigated the effects of aerobic exercise, resistance training,
or Tai Chi interventions on the cognitive function of community
dwelling older adults (>50) with no known cognitive impairment.
The exercise categories were chosen based on a scope of the available literature that found that the majority of RCTs fell into one of
these three categories. Studies required at least ten participants per
condition in order to be included in the review. We also excluded
studies if participants had been diagnosed with any cardiovascular
disease, or other signicant medical, psychiatric, or neurological
problems (see excluded studies table, Appendix C). The risk of bias
in individual studies was assessed by two independent reviewers
(Appendix D) using guidelines outlined in Section 8 of the Cochrane
Handbook.
The primary outcome of interest was cognitive function, divided
into the domains of memory and executive function. Sub-categories
were created within each domain. Memory domain sub-categories
were: recognition, immediate recall, delayed recall, face-name
recall, and paired associates. Executive function domain subcategories were: working memory, verbal uency, reasoning,
attention, and processing speed. Composite measures of cognitive function were also included. Secondary outcomes of interest
were subjective cognitive performance and activities of daily living
(ADL).
2.3. Statistical analysis
Data extraction was conducted by two independent reviewers
and cross-checked by a member of the expert panel. Review Manager Version 5.2.6 software for Windows was used to conduct the
analysis. We calculated treatment effects based on pooled data
from individual trials that were deemed clinically homogenous.
The neuropsychological measures in included articles are listed in
Tables 16. For the purpose of meta-analysis, some cognitive tests
were not included as double representation of studies in their cognitive category would compromise the validity of the outcomes. All
trials reported outcomes as continuous data. The summary statistics required for each outcome were the number of participants in
the intervention and control groups at baseline and post-test, the
mean change from baseline and the standard deviation (SD) of the
mean change. If change from baseline scores were not provided,
they were calculated using baseline and post-test mean and SDs.
Change SDs were calculated assuming zero correlation between
the measures at baseline and follow-up. Although this method may
overestimate the SD of the change from baseline, it is a conservative approach which is preferable in a meta-analysis (Levy et al.,
2012).
As pooled trials used different rating scales or tests, the
summary measure of treatment effect was the standardised
mean difference (SMD the absolute mean difference divided
by the standard deviation). Where trials used the same rating scale or test, the weighted mean difference was calculated.
Individual effect sizes were combined using the inverse variance random-effects method (Braun et al., 2009). This was
used to allow the incorporation of heterogeneity among studies. Statistical heterogeneity was assessed by the I2 test, which
describes the percentage of variability among effect estimates
beyond that expected by chance. Overall estimates of the treatment difference are presented in forest plots (Figs. 16). As
it was not possible to pool data from all included studies, a
summary of results from individual trials are outlined and presented in Tables 16.
3. Results
3.1. Included studies
Twenty-ve randomised controlled trials were eligible for inclusion with 731 participants in aerobic exercise, 304 in resistance
training, and 106 in Tai Chi exercise experimental groups; and 332
in stretching/toning, 572 in no exercise active controls, and 172
in no intervention control groups. The most common intervention was aerobic exercise. The stretching/toning control consisted
of stretching and toning or yoga exercises. The no exercise active
control groups received either health education, watched movies or
engaged in general conversation and socialising. The no intervention controls received either no contact, minimum social support,
or were placed on a waiting list. Study characteristics are presented
in Tables 16.
3.2. Aerobic exercise versus stretching/toning
Available data from individual trials were pooled for metaanalyses (Fig. 1). Despite a trend towards improved performance for
experimental versus control groups on each of the included measures, there were no signicant differences between aerobic exercise
versus stretching/toning on immediate recall (p = 0.62), delayed
recall (p = 0.16), working memory (p = 0.30), attention (p = 0.15),
or processing speed (p = 0.28). Data were not available for the
remaining outcomes of interest including recognition, face-name
recall, paired associates, verbal uency, reasoning, overall cognitive
performance, subjective cognitive measures, or ADLs. A summary
of results from individual studies (Table 1) showed signicant
improvements for aerobic exercise compared to stretching/toning
groups in three of 17 memory outcome measures reported in four
trials (Barnes et al., 2013; Erickson et al., 2011; Kramer, Hahn,
McAuley, et al., 2002; Oken et al., 2006), with signicant pre- to
post-intervention improvements for the intervention group but not
for the control group on one additional memory outcome measure
(Kramer et al., 2002). Signicant improvements for aerobic exercise
versus stretching were reported in two out of 40 separate measures of executive function in ve trials (Albinet et al., 2010; Barnes
et al., 2013; Kramer et al., 2002; Oken et al., 2006; Smiley-Oyen
et al., 2008), with signicant pre- to post-intervention improvements reported for the experimental but not for the control groups
on one additional measure of executive function (Kramer et al.,
2002). None of the included studies measured maintenance effects.
3.3. Aerobic exercise versus no exercise active control
Results from the meta-analysis (Fig. 2) revealed no significant differences between aerobic exercise and no exercise
active control groups on the measures of recognition (p = 0.51),
immediate recall (p = 1.00), delayed recall (p = 0.67), verbal uency (p = 0.58), reasoning (p = 0.28), working memory (p = 0.75),
attention (p = 0.56), processing speed (p = 0.76), or cognitive function (p = 0.26). Data were not available for face-name recall,
paired associates, subjective cognitive function or ADLs. Across
individual trials (Table 2), signicant improvements for aerobic
exercise versus active controls were reported in one out of 10
memory outcome measures (Lautenschlager et al., 2008; Legault
et al., 2011; Maki et al., 2012; Mortimer et al., 2012) and two
out of 38 measures of executive function (Barella et al., 2010;
Table 1
Characteristics of studies aerobic exercise versus stretching/toning.
Ref. author (year)
Intervention
Methods
Outcomes of interest
Albinet (2010)
EG: 12
CG: 12
Executive functiona
Additional notes
Age: 6578
Mage EG: 70.9 (4.9)
Mage CG: 70.4 (3.4)
Barnes (2013)
Double-blind
EG: Exer. Int.: 3 1 h per week for 12 weeks.
Target 6075% of max HRR
CG: Exer. Cont.: 3 1 h per week for 12 weeks
FU: PT
Immediate recallc
Delayed recallc
Verbal uencyc
Proc. speed (DSSTc , Trails Ac )
Exec function/inhibitionc
Proc. speed (UFOV)c
Attention (Trails Bc , dividedc , selectivec )
Memoryc
EG1:38
CG: 38
Age: 6585
Mage EG2: 73.6 (5.1)
Mage CG1: 71.5 (4.9)
Delayed recallc
Working memoryc
Attention (Stroopc , Cov. Orient.c )
Divided attention (UFOV)c
Proc. speed (simple RTc , choice RTc )
EG: 28
CG: 29
Age: 6579
Mage EG: 69.9 (4.6)
Mage CG: 70.5 (4.5)
CC/EI: 31
CC/EC: 32
Age: 65
Mage EG: 71.1 (5.5)
Mage CG: 73.9 (6.3)
EG: 60
CG: 60
Age: 5580
Mage EG: 67.6 (5.8)
Mage CG: 65.5 (5.4)
EG: 58
CG: 66
Age: 6075
Mage EG: 67.3 (5.2)
Mage CG: 66.0 (5.3)
Oken (2006)
Three conditions:
1. Aerobic exercise (EG)
2. Yoga (stretching/toning) (CG)
3. Wait-list control
Smiley-Oyen (2008)
Erickson (2011)
Cog. Int. = cognitive intervention; Exer. Int. = exercise intervention; Cog. Cont. = cognitive control; Exer. Cont. = exercise control; EG = experimental group; CG = control group; FU = follow up; PT = post training; Mage = mean age (SD);
DSST = digit symbol substitution test; UFOV = Useful Field of View; HRQL = Health Related Quality of Life; WCST = Wisconsin Card Sort Test; RT = reaction time; Stroop W-C = Stroop word colour; RAVLT = Rey Auditory Verbal
Learning Test; HRR = heart rate reserve.
a
Signicantly greater improvement for training compared to control.
b
Signicant training effects for experimental group from BL to PT; no signicant effect for controls.
c
No signicant intervention difference between experimental and control groups.
15
16
Table 2
Characteristics of studies aerobic exercise versus no exercise active control.
Ref. author (year)
Intervention
Methods
Outcomes of interest
Additional notes
Barella (2010)
Walking exercise
programme versus
sitting quietly control
RCT
EG: 1 20 min session (with 5 min
warm-up); 5763% of max HRR
FU: PT, and 5, 10, 15, 20, 30, 45, 60, 75, 90,
105, and 120 min post-treatment
EG: 20
CG: 20
Attention (Stroop
colourb , interferencec ,
inhibitionc )
Effects maintained at 12
month post intervention.
Immed. recallc
Delayed recalla
Proc speed (DSCT)c
Verbal uencyc
Pre-morbid IQ (CCRT)c
Cognitive function
(ADAS-Coga , CDRSa )
Recognitionc
Immediate recall
(HVLTc , LM1c )
Delayed recallc
Attention (task
switchingc , Trails BAc )
Working memory
(self-ordered pointing
taskc , 1-backc , 2-backc )
Response inhibitionc
No signicant outcomes
reported.
Delayed recallc
Verbal uencya
Reasoningc
Proc speedc
Attention (dual task
testc , Trailsc )
Clock drawingc
Lautenschlager
(2008)
Maki (2012)
Four conditions:
1. Physical activity
training (EG)
2. Health ageing (CG)
3. Cognitive training
4. Combined
intervention
Single-blind RCT
EG: 3 150 min per week for 4 months
FU: PT
Walking programme
versus educational
lectures control
RCT
EG:1 1.5 h per week for 12 weeks
FU: PT
EG: 69
CG: 69
Age: 50
Mage EG: 68.6 (8.7)
Mage CG: 68.7 (8.5)
EG: 16
CG: 17
Age: 7085
Mage EG: 77.5 (4.8)
Mage CG: 75.4 (4.8)
EG: 66
CG: 67
Age: 65
Mage EG: 71.9 (4.1)
Mage CG: 72.0 (3.9)
Mortimer (2012)
Four conditions:
1. Tai Chi
2. Walking (EG)
3. Social interaction (CG)
4. No intervention
RCT
1. 3 50 min per week for 40 weeks
2 (EG). 3 50 min per week for 40 weeks
FU: PT
EG: 30
CG: 30
Age: 6079
Mage EG: 67.8 (5.0)
Mage CG: 67.9 (6.5)
Legault (2011)
Physical activity
programme versus
education and usual care
group
Age: 6090
Mage EG: 70.1(8.5)
Mage CG: 68.5 (8.3)
Table 2 (Continued)
Ref. author (year)
Intervention
Methods
Outcomes of interest
Muscari (2010)
Exercise in community
gym versus educational
materials control
RCT
EG: 3 1 h per week for 12 months, 70%
of max HRR
FU: PT
EG: 60
CG: 60
Cognitive functiona
Williamson (2009)
1. Moderate exercise
2. Moderately-intense
exercise (EG)
3. Movie-watching
control group (CG)
RCT
1. 60% of HRR
2. (EG): single 44 min training session;
70% of HRR
FU: PT
Moderate intensity
physical activity versus
health education control
Single-blind RCT
Three phases:
1. 3 centre-based (4060 min/week) for
2 months
2. 2 centre based
sessions + 3 home-based sessions/week
for 4 months
3. Home based interventions + optional 1
or 2 centre based interventions for 6
months
FU: PT
Age: 6574
Mage EG: 68.8 (2.5)
Mage CG: 69.6 (2.8)
EG1: 20
EG2: 20
CG: 18
Age: 5064
Mage : 67.8 (7.4)
EG: 45
CG: 48
Working memoryc
Cognitive
exibility/attentiona
Response inhibition
(AUT persev. withinc ,
betweenc , rule breakc )
Working memoryc
Proc. speed (DSSTb)
Attentionc
Cognitive functionc
Improvements in DSST
were sig. associated with
improvements in chair
stand score, and balance
score.
Age: 7089
Mage EG: 76.8 (4.4)
Mage CG: 78.1 (4.1)
Netz (2007)
Additional notes
EG = experimental group; CG = control group; FU = follow up; PT = post training; Mage = mean age (SD); DSST = digit symbol substitution test; UFOV = Useful Field of View; HRQL = Health Related Quality of Life; WCST = Wisconsin
Card Sort Test; ADAS-Cog = Alzheimers Disease Assessment Scale; DSCT = Digit Symbol Coding Test; CDRS = Clinical Dementia Rating Scale; CCRT = Cambridge Contextual Reading Test; MDRS = Mattis Dementing Rating Scale;
AUT = Alternative Uses Test; HRR = heart rate reserve.
a
Signicantly greater improvement for training compared to control.
b
Signicant training effects for experimental group from BL to PT; no signicant effect for controls.
c
No signicant intervention difference between experimental and control groups.
17
18
Table 3
Characteristics of studies aerobic exercise versus no intervention.
Ref. author (year)
Intervention
Methods
Outcomes of interest
Klusmann (2010)
Three conditions:
1. Computer course
2. Exercise course (EG)
3. Control group (CG)
Double-blind
EG: 3 1.5 h per week for 6 months
FU: PT
EG: 80
CG: 69
Age: 7093
Mage EG: 73.6 (4.0)
Mage CG: 73.5 (4.3)
Maillot (2012)
EG: 15
CG: 15
Additional notes
Marmeleira (2009)
EG: 16
CG: 16
Age: 6082
Mage EG: 68.2 (6.5)
Mage CG: 68.4 (6.7)
Mortimer (2012)
Four conditions:
1. Tai Chi
2. Walking (EG)
3. Social interaction
4. No intervention
(CG)
1. 3 50 min per
week for 40 weeks
2. (EG): 3 50 min
per week for 40
weeks
FU: PT
EG: 30
CG: 30
Age: 6079
Mage EG: 67.8 (5.0)
Mage CG: 68.2 (6.5)
Oken (2006)
Three conditions:
1. Yoga
2. Aerobic exercise (EG)
3. Wait-list control (CG)
EG: 38
CG: 42
Recognitionc
Immediate recallc
Delayed recallc
Working memory (DSFc , DSBc , Rey Osterreichc , clock
drawingc )
Attention (Stroopc , Trailsc )
Verbal uency (categoriesc , Boston namingc )
Reasoningc
Cognitive functionc
No statistically signicant
changes in brain volume or
neuropsychological
performance in the walking
group compared to the
no-intervention group.
Delayed recallc
Working memoryc
Attention (Stroopc , Cov. Orient.c , CRTc )
Divided attention (UFOV)c
Proc. speedc
Age: 6585
Mage EG: 73.6 (5.1)
Mage CG: 71.2 (4.4)
EG = experimental group; CG = control group; FU = follow up; PT = post training; Mage = mean age (SD); DSST = digit symbol substitution test; UFOV = Useful Field of View; HRQL = Health Related Quality of Life; WCST = Wisconsin
Card Sort Test; ADAS-Cog = Alzheimers Disease Assessment Scale; DSCT = Digit Symbol Coding Test; CDRS = Clinical Dementia Rating Scale; CCRT = Cambridge Contextual Reading Test; MDRS = Mattis Dementing Rating Scale;
AUT = Alternative Uses Test; RT = reaction time; DSF = Digit Span Forward; DSB = Digit Span Back; CRT = Choice Reaction Time; Cov. Orient. = Covert Orienting; HRR = heart rate reserve.
a
Signicantly greater improvement for training compared to control.
b
Signicant training effects for experimental group from BL to PT; no signicant effect for controls.
c
No signicant intervention difference between experimental and control groups.
Age: 6578
Mage EG: 73.5 (4.1)
Mage CG: 73.5 (3.0)
Table 4
Characteristics of studies resistance training versus stretching/toning.
Intervention
Methods
Outcomes of interest
Additional notes
Brown (2009)
Three conditions:
1. Resistance and
balance training
exercises (EG)
2. Flexibility relaxation
programme (AC)
3. No-exercise control
(CG)
EG and AC: 2 1 h
(515 min warm-up;
40 min training; 10 min
cool-down)/week for 6
months
FU: PT
EG: 66
AC: 26
CG: 34
Paired associates
(verbalc , visualc )
Reasoningb
Attention (Trails-Bc ,
Stroopc )
Verbal uencyc
Proc speedc
Working memory
(DSFc
DSBc )
Fluid intelligence
(arithmeticb , PCb )
Cassilhas (2007)
Three conditions:
1. High intensity
training group (EG)
2. Moderate training
group
3. Warm
up + stretching control
group (CG)
EG1: 20
EG2: 19
CG: 23
Age: 6575
Mage EG1: 68.4
(0.67)
Mage EG2: 69.01
(1.1)
Mage CG: 67.04
(0.54)
Immediate recall
(ROF-IRa )
Reasoninga
Working memory
(DSFa , DSBc , ROF-Cc ,
CBTFc , CBTBa )
Attention (TPCNc ,
TPCEc )
Liu-Ambrose (2010)
Three conditions:
1. Once-weekly
resistance training
2. Twice-weekly
resistance training (EG)
3. Twice-weekly
balance and tone
training (CG)
Single-blind
EG: 2 1 h per week for
52 weeks; progressive
7RM method
FU: PT
EG1: 47
EG2: 46
CG: 42
Age: 6575
Mage EG1: 69.5 (2.6)
Mage EG2: 69.4 (3.0)
Mage CG: 69.9 (3.0)
Attention (Stroopa ,
Trails B-Ac )
Working memoryc
Performance improved
by 10.9% in the 2 RT
group, the BAT group
demonstrated 0.5%
deterioration.
Age: 6295
Mage EG: 79.5 (5.9)
Mage AC: 81.5 (6.9)
Mage CG: 78.1 (6.4)
EG = experimental group; AC = active control; CG = control group; FU = follow up; PT = post training; Mage = mean age (SD); DSST = digit symbol substitution test; UFOV = Useful Field of View; HRQL = Health Related Quality of Life;
WCST = Wisconsin Card Sort Test; ADAS-Cog = Alzheimers Disease Assessment Scale; DSCT = Digit Symbol Coding Test; CDRS = Clinical Dementia Rating Scale; CCRT = Cambridge Contextual Reading Test; MDRS = Mattis Dementing
Rating Scale; AUT = Alternative Uses Test; CBTF = Corsis block-tapping forward; CBTB = Corsis block-tapping backward; TPCN = ToulousePieron Cancellations numbers; TPCE = ToulousePieron Cancellations errors; ROF-C = Rey
Osterrieth Figure Copy; ROF-IR = Rey Osterrieth Figure Immediate Recall; RM = repetition maximum.
a
Signicantly greater improvement for training compared to control.
b
Signicant training effects for experimental group from BL to PT; no signicant effect for controls.
c
No signicant intervention difference between experimental and control groups.
19
20
Table 5
Characteristics of studies resistance training versus no exercise active control.
Intervention
Methods
Outcomes of interest
Additional notes
Brown (2009)
Three conditions:
1. Resistance and
balance training
exercises (EG)
2. Flexibility relaxation
programme (AC)
3. No-exercise control
(CG)
RCT
EG and AC: 2 1 h
(515 min warm-up;
40 min training; 10 min
cool-down)/week for 6
months
FU: PT
EG: 66
AC: 26
CG: 34
Paired associates
(verbalc , visualc )
Reasoningb
Attention (Trails-Bc ,
Stroopc )
Verbal uencyc
Proc speedc
Working memory
(DSFc
DSBc )
Fluid intelligence
(arithmeticb , PCb )
EG showed signicant
improvement in mood
compared to CG.
Age: 6295
Mage EG: 79.5 (5.9)
Mage AC: 81.5 (6.9)
Mage CG: 78.1 (6.4)
Kimura (2010)
Strength training
programme versus
health education
classes
Single-blind RCT
EG: 2 1.5 h/week for
12 weeks; 60% of 1RM
FU: PT
EG: 65
CG: 54
Age: 65
Mage EG: 73.6 (4.7)
Mage CG: 75.2 (6.3)
Executive functionc
Liu-Ambrose (2008)
Home-based resistance
and balance training
(Otago Exercsie
Program; OEP) versus
control
EG: 28
CG: 24
Age: 70
Mage EG: 81.4 (6.2)
Mage CG: 83.1 (6.3)
Attention (Stroopa ,
Trails Bc )
Working memoryc
Venturelli (2010)
Upper-body physical
training versus control
Single-blind RCT
EG: 3 30 min/week,
0.9 kg increments as
required, and walk
2/week for 6 months
FU: PT, 6 months
RCT
EG: 3 45 min for 12
weeks; 50% of
1RM-adjusted as
needed, 5362% of max
HRR
FU: PT
EG: 12
CG: 11
Age: 65
Mage EG: 83.3 (6.7)
Mage CG: 84.1 (5.8)
Cognitive functiona
Activities of daily
livinga
EG = experimental group; CG = control group; FU = follow up; PT = post training; Mage = mean age (SD); DSST = digit symbol substitution test; UFOV = Useful Field of View; HRQL = Health Related Quality of Life; WCST = Wisconsin
Card Sort Test; ADAS-Cog = Alzheimers Disease Assessment Scale; DSCT = Digit Symbol Coding Test; CDRS = Clinical Dementia Rating Scale; CCRT = Cambridge Contextual Reading Test; MDRS = Mattis Dementing Rating Scale;
AUT = Alternative Uses Test; RM = repetition maximum; HRR = heart rate reserve.
a
Signicantly greater improvement for training compared to control.
b
Signicant training effects for experimental group from BL to PT; no signicant effect for controls.
c
No signicant intervention difference between experimental and control groups.
Table 6
Characteristics of studies Tai Chi versus no exercise.
Intervention
Methods
Outcomes of interest
Additional notes
Mortimer (2012)
Four conditions:
1. Tai Chi (EG)
2. Walking
3. Social interaction
4. No intervention (CG)
Comparison: Tai Chi
versus no intervention
EG: 30
CG: 30
Recognitionb
Immediate recallb
Delayed recalla
Working memory
(DSFb , DSBb , Rey
Osterreichb , clock
drawingb )
Attention (Stroopb ,
Trails Aa , Trails Ba )
Verbal uency
(categoriesa , Boston
namingb )
Reasoningb
Cognitive functiona
Compared to CG,
participants in the Tai
Chi group showed
signicant increases in
total brain volume over
the intervention
period.
Age: 6079
Mage EG: 67.3 (5.3)
Mage CG: 68.2 (6.5)
Nguyen and Kruse, 2012
EG: 39
CG: 34
Age: 6079
Mage EG: 69.2 (5.3)
Mage CG: 68.7 (4.9)
Taylor-Piliae (2010)
First phase
EG1: 37
EG2: 39
CG: 56
Second phase
EG1: 26
EG2: 34
Verbal uencyb
Working memory
(DSFb , DSBa )
Age: 6084
Mage EG1: 70.6 (5.9)
Mage EG2: 68.5 (5.0)
Mage CG: 68.2 (6.2)
EG = experimental group; CG = control group; FU = follow up; PT = post training; Mage = mean age (SD); MIA = Meta-Memory in Adulthood; CFQ = Cognitive Failures Questionnaire; Subjective CF = subjective measures of cognitive
function.
a
Signicantly greater improvement for training compared to control.
b
No signicant intervention effects for experimental compared to control.
21
22
23
24
Fig. 2. (Continued).
measures of reasoning (p < 0.005) but not on measures of working memory (p = 0.47) or attention (0.37) (Fig. 4). Data were not
available for the remaining outcomes of interest. Results from individual studies (Table 4) revealed that resistance groups performed
signicantly better than stretching/toning controls on one out of
three measures of memory and on four out of 18 measures of
executive function. One trial reported pre- to post-intervention
improvement for the resistance group but not stretching controls
on one measure of reasoning (Brown et al., 2009). None of the three
studies in this category reported follow-up data.
25
26
Fig. 3. (Continued).
on any of the remaining 26 comparisons. Across individual trials, 15 of the 25 studies reported some signicant improvements
for exercise versus controls on measures of executive function, memory, and on composite measures of cognitive function.
Despite this, the majority of comparisons yielded no signicant
differences.
27
28
4.1. Exercise-types
4.1.1. Aerobic exercise
Our lack of consistent signicant ndings for aerobic exercise
are surprising considering conclusions of Colcombe and Kramer
(2003) and Smith et al. (2010) who reported that aerobic exercise
was associated with improvements in neurocognitive functioning,
particularly executive functions (see also Guiney and Machado,
2013). We found some supportive evidence for executive benets as differences for aerobic exercise versus no intervention
approached signicance on measures of attention; and across individual trials, aerobic exercise more reliably improved performance
on executive function tasks. Despite this our results are consistent with four reviews of aerobic RCTs that concluded that there
is a lack of consistent evidence to show that aerobic interventions
(Angevaren et al., 2008; Clifford et al., 2009; Snowden et al., 2011)
or aerobic tness (Angevaren et al., 2008; Etnier et al., 2006) result
in improved performance on cognitive tasks for older adults without known cognitive impairment. Factors that may contribute to a
lack of signicant ndings are discussed in more detail below.
4.1.2. Resistance training
Although some reviews report evidence to suggest that resistance training has cognitive benets among seniors (Liu-Ambrose
and Donaldson, 2009), the results of this review, and others (Chang
et al., 2012; Snowden et al., 2011; van Uffelen et al., 2008) fail to
show any consistent evidence for the benet of resistance training
on the cognitive function of older adults. We did nd signicant
improvements on measures of reasoning for resistance training
compared to a stretching and toning control, but no differences for
working memory or attention. Chang et al. (2012) suggested that
similar to aerobic exercise, resistance training may have differential effects on cognitive function, perhaps affecting performance on
specic executive tasks. Our ndings support this view, and may go
some way towards explaining inconsistent results because many
resistance studies fail to include measures of reasoning, or other
executive measures. Better comparability in measures of executive function across studies that examine the effects of resistance
training on cognition would bring greater clarity.
4.1.3. Tai Chi
Our results on the effect of Tai Chi on attention, processing
speed, and working memory are consistent with those of Chang
et al. (2010) who reported that Tai Chi might have task-specic benets for executive function tasks. A recent meta-analysis similarly
reported signicant benets of Tai Chi for older adults executive
functioning (Wayne et al., 2014). Interestingly, both Colcombe and
Kramer (2003) and Smith et al. (2010) reported that combining
aerobic exercise and resistance training was more effective than
aerobic exercise alone at improving performance on executive tasks
of attention and working memory. As Tai Chi combines aspects of
aerobic, resistance, and exibility training, this provides further
support to the ndings of Colcombe and Smith. More research is
required to determine the possible cognitive benets of combined
exercise programmes such as Tai Chi however as not all studies
show consistent cognitive benets (Hall et al., 2009). Our results
were based on only two studies and lacked comparison with an
active control.
4.2. Discrepancies between RCT evidence and other exercise
literature
Inconsistent results from RCTs that examine the benet of exercise on the cognitive function of older adults stands in sharp
contrast to the consistent evidence from epidemiological, crosssectional, and neuroimaging research. There are however a number
29
30
Conicts of interest
All authors declare that we have no conicts of interest.
Acknowledgements
We would like to thank Dr Joanna McHugh for her edits. MK was
employed by the Alzheimer Society of Ireland during the writing of
this paper.
31