Tai Chi and the Protection of Cognitive Ability A Systematic Review of Prospective Studies in Healthy Adults Guohua Zheng, MD, Feiwen Liu, MS, Shuzhen Li, MS, Maomao Huang, MS, Jing Tao, MD, Lidian Chen, MD Context: Age-related cognitive decline has become an important public health issue. Tai Chi may be an effective intervention to protect the cognitive ability of healthy adults, but its effects are uncertain. This study systematically evaluated the protective effects of Tai Chi on healthy adults’ cognitive ability.
Evidence acquisition: A systematic review of prospective controlled trials comparing Tai Chi with usual physical activities for cognitive ability maintenance among healthy adults was conducted. Seven electronic databases were searched from their inception to December 31, 2013. Data analysis and bias risk evaluation were conducted in 2014. Evidence synthesis: Nine studies, including four RCTs and five non-randomized controlled trials, with 632 participants were identified. Global cognitive function was measured using the MiniMental State Examination, Mattis Dementia Rating Scale (MDRS), or event-related potential 300 in three studies; attention was measured by the MDRS attention score, hands and feet alternating movement time, or response time in three studies; learning and memory were assessed by MDRS memory score, Wechsler Adult Intelligence Scale, or Auditory Verbal Learning Test in three studies; emotion and perception were measured using arm stability and mental rotation in one study; and execution was measured by Trail Making Test, Stroop Test, and Clock Drawing Test in four studies. Tai Chi showed a positive effect on most outcomes of various cognitive realms. Conclusions: Compared with usual physical activities, Tai Chi shows potential protective effects on healthy adults’ cognitive ability. Large RCTs with more rigorous designs are needed to fully evaluate and confirm its potential benefits. (Am J Prev Med 2015;49(1):89–97) & 2015 Published by Elsevier Inc. on behalf of American Journal of Preventive Medicine
Context
B
y 2050, the proportion of the population aged 460 years is expected to double worldwide, from approximately 11% in 2000 to 22%, and the absolute number will increase from 605 million to two billion.1 With a rapidly aging society worldwide, agerelated cognitive decline has become an important public health issue. Cognitive decline can cause a variety of symptoms, such as forgetfulness, attention decline, and problem-solving capability decline. If left untreated, these
From the College of Rehabilitation Medicine, Fujian University of Traditional Chinese Medicine, Fuzhou, China Address correspondence to: Lidian Chen, MD, Fujian University of Traditional Chinese Medicine, HuaTuo Road, Fuzhou 350122, China, 13305001237. E-mail: [email protected]. 0749-3797/$36.00 http://dx.doi.org/10.1016/j.amepre.2015.01.002
symptoms often deteriorate to serious disabilities, such as cognition impairment and dementia, or even Alzheimer disease. It is estimated that in people aged 65 years and older, as many as 10%–20% have mild cognitive impairment, which is a transitional stage between the normal aging process and dementia.2,3 More than 10% of mild cognitive impairment patients convert to Alzheimer disease annually.4 Currently, there is no consensus on effective pharmacologic interventions for cognitive decline,5 and there is growing interest in behavioral interventions.6 Many studies have suggested that regular physical exercise is beneficial in maintaining cognitive ability.7,8 Tai Chi (TC), also known as Tai Chi Chuan or Taijiquan,9 is a traditional Chinese exercise that incorporates body movement, breath, and attention training, which has been practiced to maintain health for hundreds of years in China.10 The practice of TC consists of a
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slow, continuous flow of body positions from one pattern to the next, which promotes proper body posture, flexibility, relaxation, and mental concentration,11 and involves training of visual spatial processing, attention, executive ability, and episodic memory as well.12 It may, therefore, be beneficial for cognitive ability. Although several studies13,14 have reported the effects of TC on cognitive outcomes in various populations, the evidence remains limited regarding whether TC might protect cognitive ability in healthy adults. This systematic review evaluates TC as an intervention in order to determine whether it exerts protective effects in terms of global cognition, attention, learning and memory, and executive, emotion, and perception ability.
Evidence Acquisition Selection and Identification of Studies To identify pertinent articles, a systematic electronic literature search was performed in the Cochrane Library (Issue 4, 2013), PubMed, Science Citation Index, Embase, Chinese Scientific Journal Database, Wanfang Data Knowledge Service Platform, and China National Knowledge Information database from their inception to December 2013 by two reviewers independently. Search terms included Tai Chi, Taiji, Tai Chi Chuan, Taiji Quan, awareness, comprehension, learning, emotion, intuition, cognit*, compare, control, and related terms. Chinese counterpart terms were applied for the Chinese databases. The unpublished literature was searched using the Chinese Master’s Theses Full-Text Database, China Doctor Dissertation Full-Text Database, and China Proceedings of Conference Full-Text Database. Hand searches were conducted among the retrieved articles for additional references. The search strategy is detailed in Appendix Table 1 (available online). All searched records were imported into a reference management software (Note Express), which facilitated elimination of duplicate records. Eligible articles were selected and checked independently according to the inclusion criteria by two reviewers. Full-text articles that could not be accessed directly were obtained by a document delivery service or by contacting the original authors. Missing data were obtained from the original authors if possible. Any disagreements were solved by discussion with the third reviewer.
Inclusion Criteria Studies were identified for the present systematic review when they met the following inclusion criteria: 1. Study design: Parallel controlled studies comparing TC with usual
physical activities for cognitive ability maintenance were included, regardless of randomized or non-randomized design. There were no restrictions on randomization, blinding, publication status, or language. 2. Participants: Study populations consisted of healthy adults, regardless of sex, age, or racial and ethnic groups. 3. Interventions: TC exercises, regardless of genre (e.g., Chen, Yang, Sun) or style (e.g., eight-style, 16-style, 24-style, 48-
style), were practiced by the treatment group for at least 6 weeks. 4. Control condition: No specific exercise intervention was used, but usual physical activities were maintained. 5. Outcomes: Global cognitive ability or at least one domain of specific cognitive abilities (attention, learning and memory, language, emotion and perception, and execution) was assessed by neuropsychological tests or other objective measurements.
Data Extraction and Quality Assessment Two reviewers independently extracted data from the eligible studies. The extracted data included basic information from the articles, demographic characteristics of participants, methodological characteristics, type and process of TC exercise, control conditions, outcomes, and adverse events. The accuracy of the results was checked by another reviewer. The methodological quality of the included studies was assessed using the tool developed by the Cochrane Collaboration.15 The following types of bias were assessed: selection bias (random sequence generation and allocation concealment); performance bias (blinding of participants and personnel); detection bias (blinding of outcome assessment); attrition bias (incomplete outcome data); reporting bias (selective outcome reporting); and other bias. In cases of disagreement between two reviewers, a consensus was achieved by discussion with the third reviewer.
Statistical Analysis The extracted outcomes were classified into five large groups according to cognitive domain in 2014. RevMan, version 5.2, provided by the Cochrane Collaboration was used for statistical analysis. Data were summarized using the relative risk and 95% CI for binary outcomes or the mean difference (MD) or standardized mean difference (SMD) and 95% CI for continuous outcomes.16 Pooled effects were analyzed using the fixed-effects model if the extracted outcomes were available and had good homogeneity; otherwise, a random-effects model was used if possible. Heterogeneity among studies was explored using chi-square analysis, with the significance level set at po0.05 and the I2 value.
Evidence Synthesis Study Selection According to the initial search strategy, 650 records were identified from the relevant databases and 97 duplicate records were excluded. Among the 553 potential articles, 528 were excluded by reading the title and abstract. Consequently, 17 articles were further excluded from the remaining 25 full-text articles because they did not meet the inclusion criteria. Finally, nine articles were included, one of which was identified from the reference lists of the included articles. The reasons for article exclusion are listed in Appendix Table 2 (available online). Nine studies were assessed in this systematic review, including four RCTs17–20 and five non-randomized controlled trials.21–25 The literature searching and screening process is described in Figure 1. www.ajpmonline.org
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Study Characteristics All nine included studies were designed to compare TC with usual physical activities, involving a total of 632 healthy adults. All except two studies22,23 focused on middle-aged and older adults with ages ranging from 45 to 79 years. Six studies17,21–25 were conducted in China, one18 in Vietnam, and two19,20 in the U.S. In the included studies, TC intervention varied widely in practice frequency, duration, and style. The duration of TC practice ranged from 6 weeks to 3 years, and the frequency varied from one to seven sessions per week and 30 to 90 minutes per session. The specific style of TC was not provided in four studies,17,18,21,23 whereas the five other studies reported that 12-form Yang style,19 12-form Sun style,20,25 24-form simplified TC,22 or 108-form TC24 was applied. Outcomes from six cognitive domains, which included global cognitive ability, attention, learning and memory, language, emotion and perception, and execution, were assessed using the Mini-Mental State Examination (MMSE),20 Category Verbal Fluency Test (CVFT),19 Clock Drawing Test (CDT),17 Trail Making Test (TMT),18 Stroop Test (ST),22 Mattis Dementia Rating Scale (MDRS),17 and response time.21 The characteristics of the included articles are summarized in Table 1.
Risk of Bias in Included Studies The methodologic quality of the included studies is detailed in Appendix Table 3 (available online). Of the CDFD n=50
CMFD n=75
CPCD n=77
VIP n=10
nine included studies, four reported “random allocation among participants,” but none described the randomization procedures and allocation concealment of the randomization sequence. Only one study20 reported assessor blinding. Intention-to-treat analysis was performed in one study.17 Only one study17 reported loss to follow-up or study withdrawal and clearly described the method of data collection. Therefore, these studies could not be judged to be free of bias from incomplete outcome data. Although the study protocol was not available in all included studies, it was clear that the outcomes listed in the Methods section of each article could be compared with the reported results; therefore, these studies were judged to be at low risk of bias from selective reporting of outcomes. We judged one study25 as “unclear” in terms of freedom from other bias because there was no evidence of statistical testing of baseline characteristics between the comparison groups. Overall, all studies were judged to have a high risk of bias with low methodological quality.
Measures of Effect Global Cognitive Ability Two studies reported on global cognitive ability assessed using MDRS17 or event-related potential 300 (P300).23 We did not meta-analyze these two studies together because of the diversity of outcome measures. However, their separate results showed that TC resulted in an obvious improvement SCI n=103
Embase n=92
Pubmed n=69
Cochrane n=151
97 articles excluded because of reduplication, according to title and author names.
Screening
Potential eligible articles, n=25.
Eligibility
Potentially relevant articles, n=553.
Full-text articles for more detailed evaluation, n=26.
Included
Identification
Wanfang n=23
91
Eligible articles, n=9.
Excluded based on title and abstract, n=528: narrative reviews, n=68; irrelevant to Tai Chi, n=274; irrelevant to cognition, n=153; investigation, n=7; comments, n=22; animal experiments, n=4. 1 article identified from scanning reference of relevant narrative. 17 full-text articles excluded: duplicate publication, n=1; participants were not health adults, n=6; Tai Chi plus other interventions, n=1; no usual physical activity control group, n=4; self controlled trial, n=1; unacceptable cognitive outcomes, n=4.
Included quantitative synthesis, n=6.
Figure 1. Literature search and selection flow diagram showing reasons for exclusion. CDFD, China Doctor Dissertation Full-Text Database; CMFD, Chinese Master’s Theses Full-Text Databases; CPCD, China Proceedings of Conference Full-text Database; SCI, Science Citation Index; VIP, Chinese Scientific Journal Database.
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Table 1. Literature Characteristics Author/ year/ Country
Compare Study design
Sample (I/C)
Mortimer (2012),17 China
RCT
30/30
Nguyen (2012),18 Vietnam
RCT
Taylor (2010),19 America
Participants (age/ years, sex)
Tai Chi/ duration
Outcomes/ measurements
UPA
50 minutes 3 times/ week40 weeks
Global cognition: MDRS Memory: WAISDS, CVFT, AVLT Execution: TMT, CDT, ST
TC (no specific)
UPA
60 minutes 2 times/ week24 weeks
Execution: TMT
Age range: 460 years Sex: male29, female 64;
TC (12-form Yang)
UPA
45 minutes 7 times/ week24 weeks
Memory: WAISDS, CVFT
28/27
Age range: 460 years
TC (12-form Sun)
UPA
40 minutes 3 times/ week20 weeks
Global cognition: MMSE
NRCT
53/48
Age range: 45–74 years Sex: male 49, female 52;
TC (no specific)
UPA
424 weeks
Attention: response time, HFAM, Emotion: arm stability Perception: mental rotation
Liu (2011),22 China
NRCT
31/23
Sex: male 16, female 38
TC (24-form simplified)
UPA
45 minutes 1 time/ week16 weeks
Execution: ST
Lan (2009),23 China
NRCT
17/30
Age: T: 21.33⫾1.75 years; C: 21.23⫾1.52 years
TC (no specific)
UPA
55 minutes 3 times/ week6 weeks
Global cognition: P300
Man (2010),24 China
NRCT
42/44
Age range: 460 years
TC (Ng style)
UPA
45 minutes 3 times/ week3 years
Attention: CTT Memory: RBMT, HKLLT
Wei (2013),25 China
NRCT
22/18
Age: 52⫾6 years
TC (Yang, Wu, Sun, Chen)
UPA
30–90 minutes 7 times/ week14 years
Global cognition: MRI Execution: ANT
Intervention
Control
Age range: 60–70 years Sex: male 20, female 40
TC (no specific)
48/48
Age range: 60–79 years Sex: male 48, female 48
RCT
37/56
Tsai (2013),20 America
RCT
Zhang (2006),21 China
AVLT, Auditory Verbal Learning Test; ANT, Attention Network Test; C, control group; CDT, Clock Drawing Test; CTT, Color Trail Test; CVFT, Category Verbal Fluency Test; HFAM, hands and feet alternating movement; HKLLT, Hong Kong List Learning Test; I, intervention group; MDRS, Mattis Dementia Rating Scale; MRI, magnetic resonance imaging; MMSE, Mini-Mental State Examination; NR, not reported; NRCT, non-randomized controlled trial; RBMT, Rivermead Behavioral Memory Test; ST, Stroop Test; P300, event-related potential 300; TC, Tai Chi; TMT-A, Trail Making Test Part A; TMT-B, Trail Making Test Part B; UPA, usual physical activity; WAIS-DS, Wechsler Adult Intelligence Scale–Digit Span.
in MDRS scores (MD¼4.59, 95% CI¼1.37, 7.81, p¼0.005) and a reduction in P300 reaction time (MD¼–33.08, 95% CI¼–55.99, –10.17, p¼0.005) and P300 latency period (MD¼–20.54, 95% CI¼–39.15, –1.93, p¼0.03) compared with the usual physical activities (Table 2). One study20 reported that TC training participants had higher MMSE scores than those in the usual physical activities group, but the difference was not significant (p¼0.096).
Attention Attention was reported in three studies17,21,24 comparing TC exercise with the usual physical activities. One
study17 reported the significant improvement in MDRS attention score following TC exercise (MD¼0.52, 95% CI¼0.08, 0.96, p¼0.02). One study21 reported that TC resulted in an obvious improvement of attention focus time (MD¼1.48, 95% CI¼1.06, 1.90, po0.0001); time of correct hands and feet alternating movement (HFAM; MD¼15.62, 95% CI¼8.91, 22.33, po0.00001); and mean HFAM time (MD¼14.56, 95% CI¼8.10, 21.02, po0.00001) as well as a clear decrease in attention dispersal time (MD¼–7.68, 95% CI¼–9.63, –5.37, po0.0001); mean response time (MD¼–136.19, 95% CI¼–198.81, –73.57, po0.0001); and total HFAM time
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Table 2. Tai Chi Exercise on Global Cognitive Ability Compared With Usual Physical Activity
Measure MDRS score
No. of studies
No. of participants
1: Mortimer (2012)17
MD (95% CI)
60 (I: 30; C: 30)
4.59 (1.37, 7.81)
Test for overall effect (p-value) 0.005
P300 response time (ms)
1: Lan (2009)
23
47 (I: 17; C: 30)
–33.1 (–55.99, –10.17)
0.005
P300 latency period (ms)
1: Lan (2009)23
47 (I: 17; C: 30)
–20.5 (–39.15, –1.93)
0.03
P300 wave amplitude
1: Lan (2009)23
47 (I: 17; C: 30)
0.17 (–1.46, 1.80)
0.84
Note: Boldface indicates statistical significance (po0.05). C, control group; I, intervention group; MDRS, Mattis Dementia Rating Scale; ms, milliseconds; MD, mean difference.
(MD¼–209.03, 95% CI¼–325.34, –65.72, p¼0.004). However, no significant changes were found for optimal response time in the study (Table 3). Another study24 also reported a significantly positive effect of TC exercise on attention, which was evaluated by the Color Trail Test (A-1 and 2) (po0.01; no available data were extracted).
However, another study24 reported that the TC group had better memory ability performance than the usual physical activities control group as assessed by the Rivermead Behavioral Memory Test (RBMT-CV) and Hong Kong List Learning Test (HKLLT) (po0.01; no available data were extracted).
Learning and Memory
Emotion and Perception
Comparing with the usual physical activities, TC exercise significantly improved the level of learning and memory as assessed by MDRS memory score (one trial,17 MD¼1.01, 95% CI¼0.02, 2.0, p¼0.05); Wechsler Adult Intelligence Scale–Digit Span (WAIS-DS; forward) (two trials,17,19 MD=–0.46, 95% CI=–0.89, –0.03, p=0.04); and Auditory Verbal Learning Test (AVLT; delayed recognition) (one trial,17 MD¼2.01, 95% CI¼0.37, p¼0.02). Other measurements, including CVFT, WAISDS (backward), and AVLT (immediate recall), were not shown to have a significant difference (Table 4).
One trial21 with 93 participants reported on emotion and perception ability as assessed by measuring arm stability and mental rotation time. Compared with the usual physical activities, TC exercise significantly improved arm stability (MD¼3.71, 95% CI¼0.86, 6.56, p¼0.01) and mental rotation time (MD¼–0.39, 95% CI¼–0.77, –0.01, p¼0.05) (Table 5).
Execution Three trials17,18,22 involving 217 participants reported on execution ability assessed by TMT, ST, and CDT (Table 6). Compared with the usual physical activities, TC exercise
Table 3. Tai Chi Exercise on Attention Compared With Usual Physical Activity
Measure
No. of studies
No. of participants
MD (95% CI)
Test for overall effect (p-value)
Time of attention focus (seconds)
1: Zhang (2006)21
93 (I: 50; C: 43)
1.48 (1.06, 1.90)
o0.00001
No. of times attention dispersed (M)
1: Zhang (2006)21
93 (I: 50; C: 43)
–7.68 (–9.63, –5.37)
o0.00001
Response time (seconds; M)
1: Zhang (2006)21
93 (I: 50; C: 43)
–136.19 (–198.81, –73.57)
o0.0001
Optimal response time (seconds)
21
1: Zhang (2006)
93 (I: 50; C: 43)
Total time of HFAM (seconds)
1: Zhang (2006)21
93 (I: 50; C: 43)
No. of times HFAM done correctly (M)
1: Zhang (2006)21
93 (I: 50; C: 43)
15.62 (8.91, 22.33)
o0.00001
Mean time of HFAM (seconds)
1: Zhang (2006)21
93 (I: 50; C: 43)
14.56 (8.10, 21.02)
o0.00001
60 (I: 30; C: 30)
0.52 (0.08, 0.96)
0.02
MDRS attention score (M)
17
1: Mortimer (2012)
–31.17 (–67.78, 5.44) –209.03 (–325.34, –65.72)
0.10 0.004
Note: Boldface indicates statistical significance (po0.05). C, control group; HFAM, hands and feet alternating movement; I, intervention group; MD, mean difference; MDRS, Mattis Dementia Rating Scale.
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Table 4. Tai Chi Exercise on Learning and Memory Compared With Usual Physical Activity Heterogeneity Measure (score)
No. of studies
No. of participants
MD (95% CI)
I²
p-value
Test for overall effect (p-value)
MDRS memory score
1: Mortimer (2012)17
60 (I: 30; C: 30)
1.01 (0.02, 2.0)
—
—
0.05
CVFT, animals
2: Mortimer (2012),17 Taylor (2010)19
153 (I: 67; C: 86)
–1.13 (–2.47, 0.21)
84%
0.01
0.10
WAIS-DS, forward
2: Mortimer (2012),17 Taylor (2010)19
153 (I: 67; C: 86)
–0.46 (–0.89, –0.03)
71%
0.07
0.04
WAIS-DS, backward
2: Mortimer (2012),17 Taylor (2010)19
153 (I: 67; C: 86)
0.21 (–0.47, 0.89)
0%
0.75
0.55
AVLT, immediate recall
1: Mortimer (2012)17
60 (I: 30; C: 30)
0.38 (–0.74, 1.5)
—
—
0.51
AVLT, delayed recall
1: Mortimer (2012)17
60 (I: 30; C: 30)
1.22 (–0.4, 2.84)
—
—
0.14
AVLT, delayed recognition
1: Mortimer (2012)17
60 (I: 30; C: 30)
2.01 (0.37, 3.65)
—
—
0.02
Note: Boldface indicates statistical significance (po0.05). AVLT, Auditory Verbal Learning Test; C, control group; CVFT, Category Verbal Fluency Test; DS, Digit Span test; I, intervention group; MD, mean difference; MDRS, Mattis Dementia Rating Scale; WAIS, Wechsler Adult Intelligence Scale.
resulted in a positive improvement on execution ability as measured by TMT-B (two trials,17,18 MD=–16.02, 95% CI=–18.66, –13.37, po0.0001), ST-word (two trials,17,22 MD=–0.46, 95% CI=–0.9, –0.03, p=0.04), and ST-color– word (two trials,17,22 MD=–1.73, 95% CI=–3.42, –0.04, p=0.04). There was, however, no significant change in values of TMT-A, ST-color, and CDT. Another study25 reported improvement in executive ability assessed by the Attention Network Test. In addition, the brain was reshaped through TC exercise, which was associated with greater intensity of TC practice.
Safety and Adverse Events No adverse events were reported in the included studies.
Discussion This systematic review examined the protective effects of TC exercise on the cognitive ability of healthy adults.
Nine studies involving 632 participants were included in this review. All studies were designed to compare TC exercise with usual physical activities. As a whole, the included studies were of low quality. We attempted to contact the original authors by telephone and e-mail for further information. However, most replies were unsatisfactory or had little ability to resolve our questions, and some of the authors did not reply or could not be contacted. Nevertheless, the results of this review showed that TC exercise could significantly improve the majority of outcomes of global cognitive ability, attention, learning and memory, language, emotion and perception, and execution in healthy adults. It may, therefore, be helpful in protecting the cognitive ability of healthy adults. The benefits of exercise on cognitive ability have been widely recognized. Studies have shown that people who were more active in midlife and late life have a lower risk of global cognitive decline.26,27 People who walk more than two miles per day have a significantly lower risk of
Table 5. Tai Chi Exercise on Emotion and Perception Compared With Usual Physical Activity
Measure Emotion: Arm stability (score) Perception: Mental rotation (score)
No. of studies
No. of participants
MD (95% CI)
Test for overall effect (p-value)
1: Zhang (2006)21
93 (I: 50; C: 43)
3.71 (0.86, 6.56)
0.01
21
93 (I: 50; C: 43)
–0.39 (–0.77, –0.01)
0.05
1: Zhang (2006)
Note: Boldface indicates statistical significance (po0.05). C, control group; I, intervention group; MD, mean difference.
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Table 6. Tai Chi Exercise on Execution Compared With Usual Physical Activity Heterogeneity Measure (score)
No. of studies
No. of participants
MD (95% CI)
I²
p-value
Test for overall effect (p-value)
TMT-A
2: Nguyen (2012),18 Mortimer (2012)17
133 (I: 69; C: 64)
6.88 (–1.74, 15.50)
0%
0.84
TMT-B
2: Nguyen (2012),18 Mortimer (2012)17
133 (I: 69; C: 64)
–16.02 (–18.66, –13.37)
81%
0.02
ST-word (CWT-A)
2: Liu (2011),22 Mortimer (2012)17
144 (I: 61; C: 53)
–0.46 (–0.90, –0.03)
48%
0.16
0.04
ST-color (CWT-B)
2: Liu (2011),22 Mortimer (2012)17
144 (I: 61; C: 53)
–0.02 (–0.89, 0.84)
0%
0.48
0.96
ST-color–word (CWT-C)
2: Liu (2011),22 Mortimer (2012)17
144 (I: 61; C: 53)
–1.73 (–3.42, –0.04)
58%
0.12
0.04
CDT
1: Mortimer (2012)17
60 (I: 30; C: 30)
–0.62 (–2.79, 1.55)
—
—
0.58
0.12 o0.00001
Note: Boldface indicates statistical significance (po0.05). C, control group; CDT, Clock Drawing Test; I, intervention group; ST, Stroop Test; TMT-A, Trail Making Test Part A; TMT-B, Trail Making Test Part B; MD, mean difference.
developing dementia compared with those who walk less than one mile per day.28 TC is a traditional Chinese exercise that has been developed since the 17th century. During the process of development, TC was differentiated into five main styles: Chen, Yang, Wu, Sun, and simplified TC. In recent years, TC has become a popular exercise worldwide, and research on its benefits is flourishing. However, the majority of these studies have focused on the effects of TC on muscular strength,29 balance,30 the vestibular system,31 prevention of falls,32 physical function,33 and quality of life.34 Currently, a limited number of studies have assessed the use of TC to preserve the cognitive ability of older adults. As a form of physical exercise, TC is a light to moderate– intensity aerobic activity with estimated METs between 1.5 and 4.0.35,36 Its exercise intensity can be easily adjusted by controlling the speed and postural height. Theoretically, aerobic exercise could promote cognitive ability by directly improving the cerebral circulation and the action of neurotransmitters. In addition, as a mind–body exercise, TC involves learning and memorization of new skills and movement patterns, and sustaining attention focus, which could be helpful to train working memory, divided attention, cognitive flexibility, and overall executive ability. Two previous reviews systematically assessed the effect of TC on cognitive ability in an older population with or without cognitive impairment and suggested small to moderate improvements in executive ability, language, learning, and memory. However, the interventions in the control groups were diverse in their included studies, in which other exercises, handicrafts, education and social activities, rehabilitation, and other interventions were July 2015
applied.37,38 Therefore, the protective efficacy of TC compared to the usual physical activities for maintaining cognitive ability among healthy adults remains ambiguous. The present review was designed to assess the efficacy of TC exercise on the cognitive ability by comparison with the usual physical activities. Although only nine eligible studies were included in this review, pooled analyses were not performed, owing to use of different outcomes and variability in the amount of exercise, number of participants, and methodological quality among the included studies. TC in these studies showed a positive association with the majority of outcomes of global cognitive ability, attention, learning and memory, language, emotion and perception, and execution among healthy adults.
Limitations and Recommendations for Future Research This study had several limitations. First, the number of studies and the clinical heterogeneity of the outcomes made their synthesis and meta-analysis difficult, and publication bias was not explored by funnel plot analysis because of an insufficient number of included studies.39 Second, the overall methodological quality of the included studies was low. If more definitive conclusions are to be drawn, large-scale and high-quality RCTs should be encouraged. Third, subjective assessments were used in most studies. In order to better evaluate the effects of TC exercise on cognitive ability, future studies should make use of various objective detection methods and instruments (e.g., event-related potential, functional magnetic resonance imaging). In addition, the
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Type I error was likely inflated given great differences in the design and outcomes reported among different studies, whereas significant results were observed only in one or two studies. Finally, limitations were also seen in the lack of TC standardization, with variations in the intensity of each session, styles, and teaching quality. Standardized TC exercise is useful in ensuring good homogeneity and demonstrating its effectiveness. Therefore, future studies should not only report important design features (e.g., blinding, randomization) but also illustrate the features relevant to TC specifically.
Conclusions In order to make more definitive conclusions regarding the potential protective effects of TC on the cognitive ability of healthy adults, more rigorously designed, largescale RCTs are required in future research. The authors thank Dr. Li Ge (School of Nursing, Fujian University of Traditional Chinese Medicine) for her helpful evaluation and revision of the second revised manuscript. This systematic review is supported by the Collaboration Innovation Center for Rehabilitation Technology (Number 1 Collaboration Center [2012]) and the Rehabilitation Research Center for Traditional Chinese Medicine, State Administration of Traditional Chinese Medicine of the People’s Republic of China. ZGH, TJ, and CLD conceived of the study, LFW drafted the manuscript, and ZGH revised it and wrote several sections of this manuscript. LSZ and HMM were the research assistants who helped with data extraction, quality assessment, and other aspects of the study. All authors contributed to the writing of the manuscript and have read and approved the final version for publication. ZGH and LFW contributed equally to this study. No financial disclosures were reported by the authors of this paper.
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Appendix Supplementary data Supplementary data associated with this article can be found at http://dx.doi.org/10.1016/j.amepre.2015.01.002.
Evidence acquisition: A systematic review of prospective controlled trials comparing Tai Chi with usual physical activities for cognitive ability maintenance among healthy adults was conducted. Seven electronic databases were searched from their inception to December 31, 2013. Data analysis and bias risk evaluation were conducted in 2014. Evidence synthesis: Nine studies, including four RCTs and five non-randomized controlled trials, with 632 participants were identified. Global cognitive function was measured using the MiniMental State Examination, Mattis Dementia Rating Scale (MDRS), or event-related potential 300 in three studies; attention was measured by the MDRS attention score, hands and feet alternating movement time, or response time in three studies; learning and memory were assessed by MDRS memory score, Wechsler Adult Intelligence Scale, or Auditory Verbal Learning Test in three studies; emotion and perception were measured using arm stability and mental rotation in one study; and execution was measured by Trail Making Test, Stroop Test, and Clock Drawing Test in four studies. Tai Chi showed a positive effect on most outcomes of various cognitive realms. Conclusions: Compared with usual physical activities, Tai Chi shows potential protective effects on healthy adults’ cognitive ability. Large RCTs with more rigorous designs are needed to fully evaluate and confirm its potential benefits. (Am J Prev Med 2015;49(1):89–97) & 2015 Published by Elsevier Inc. on behalf of American Journal of Preventive Medicine
Context
B
y 2050, the proportion of the population aged 460 years is expected to double worldwide, from approximately 11% in 2000 to 22%, and the absolute number will increase from 605 million to two billion.1 With a rapidly aging society worldwide, agerelated cognitive decline has become an important public health issue. Cognitive decline can cause a variety of symptoms, such as forgetfulness, attention decline, and problem-solving capability decline. If left untreated, these
From the College of Rehabilitation Medicine, Fujian University of Traditional Chinese Medicine, Fuzhou, China Address correspondence to: Lidian Chen, MD, Fujian University of Traditional Chinese Medicine, HuaTuo Road, Fuzhou 350122, China, 13305001237. E-mail: [email protected]. 0749-3797/$36.00 http://dx.doi.org/10.1016/j.amepre.2015.01.002
symptoms often deteriorate to serious disabilities, such as cognition impairment and dementia, or even Alzheimer disease. It is estimated that in people aged 65 years and older, as many as 10%–20% have mild cognitive impairment, which is a transitional stage between the normal aging process and dementia.2,3 More than 10% of mild cognitive impairment patients convert to Alzheimer disease annually.4 Currently, there is no consensus on effective pharmacologic interventions for cognitive decline,5 and there is growing interest in behavioral interventions.6 Many studies have suggested that regular physical exercise is beneficial in maintaining cognitive ability.7,8 Tai Chi (TC), also known as Tai Chi Chuan or Taijiquan,9 is a traditional Chinese exercise that incorporates body movement, breath, and attention training, which has been practiced to maintain health for hundreds of years in China.10 The practice of TC consists of a
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slow, continuous flow of body positions from one pattern to the next, which promotes proper body posture, flexibility, relaxation, and mental concentration,11 and involves training of visual spatial processing, attention, executive ability, and episodic memory as well.12 It may, therefore, be beneficial for cognitive ability. Although several studies13,14 have reported the effects of TC on cognitive outcomes in various populations, the evidence remains limited regarding whether TC might protect cognitive ability in healthy adults. This systematic review evaluates TC as an intervention in order to determine whether it exerts protective effects in terms of global cognition, attention, learning and memory, and executive, emotion, and perception ability.
Evidence Acquisition Selection and Identification of Studies To identify pertinent articles, a systematic electronic literature search was performed in the Cochrane Library (Issue 4, 2013), PubMed, Science Citation Index, Embase, Chinese Scientific Journal Database, Wanfang Data Knowledge Service Platform, and China National Knowledge Information database from their inception to December 2013 by two reviewers independently. Search terms included Tai Chi, Taiji, Tai Chi Chuan, Taiji Quan, awareness, comprehension, learning, emotion, intuition, cognit*, compare, control, and related terms. Chinese counterpart terms were applied for the Chinese databases. The unpublished literature was searched using the Chinese Master’s Theses Full-Text Database, China Doctor Dissertation Full-Text Database, and China Proceedings of Conference Full-Text Database. Hand searches were conducted among the retrieved articles for additional references. The search strategy is detailed in Appendix Table 1 (available online). All searched records were imported into a reference management software (Note Express), which facilitated elimination of duplicate records. Eligible articles were selected and checked independently according to the inclusion criteria by two reviewers. Full-text articles that could not be accessed directly were obtained by a document delivery service or by contacting the original authors. Missing data were obtained from the original authors if possible. Any disagreements were solved by discussion with the third reviewer.
Inclusion Criteria Studies were identified for the present systematic review when they met the following inclusion criteria: 1. Study design: Parallel controlled studies comparing TC with usual
physical activities for cognitive ability maintenance were included, regardless of randomized or non-randomized design. There were no restrictions on randomization, blinding, publication status, or language. 2. Participants: Study populations consisted of healthy adults, regardless of sex, age, or racial and ethnic groups. 3. Interventions: TC exercises, regardless of genre (e.g., Chen, Yang, Sun) or style (e.g., eight-style, 16-style, 24-style, 48-
style), were practiced by the treatment group for at least 6 weeks. 4. Control condition: No specific exercise intervention was used, but usual physical activities were maintained. 5. Outcomes: Global cognitive ability or at least one domain of specific cognitive abilities (attention, learning and memory, language, emotion and perception, and execution) was assessed by neuropsychological tests or other objective measurements.
Data Extraction and Quality Assessment Two reviewers independently extracted data from the eligible studies. The extracted data included basic information from the articles, demographic characteristics of participants, methodological characteristics, type and process of TC exercise, control conditions, outcomes, and adverse events. The accuracy of the results was checked by another reviewer. The methodological quality of the included studies was assessed using the tool developed by the Cochrane Collaboration.15 The following types of bias were assessed: selection bias (random sequence generation and allocation concealment); performance bias (blinding of participants and personnel); detection bias (blinding of outcome assessment); attrition bias (incomplete outcome data); reporting bias (selective outcome reporting); and other bias. In cases of disagreement between two reviewers, a consensus was achieved by discussion with the third reviewer.
Statistical Analysis The extracted outcomes were classified into five large groups according to cognitive domain in 2014. RevMan, version 5.2, provided by the Cochrane Collaboration was used for statistical analysis. Data were summarized using the relative risk and 95% CI for binary outcomes or the mean difference (MD) or standardized mean difference (SMD) and 95% CI for continuous outcomes.16 Pooled effects were analyzed using the fixed-effects model if the extracted outcomes were available and had good homogeneity; otherwise, a random-effects model was used if possible. Heterogeneity among studies was explored using chi-square analysis, with the significance level set at po0.05 and the I2 value.
Evidence Synthesis Study Selection According to the initial search strategy, 650 records were identified from the relevant databases and 97 duplicate records were excluded. Among the 553 potential articles, 528 were excluded by reading the title and abstract. Consequently, 17 articles were further excluded from the remaining 25 full-text articles because they did not meet the inclusion criteria. Finally, nine articles were included, one of which was identified from the reference lists of the included articles. The reasons for article exclusion are listed in Appendix Table 2 (available online). Nine studies were assessed in this systematic review, including four RCTs17–20 and five non-randomized controlled trials.21–25 The literature searching and screening process is described in Figure 1. www.ajpmonline.org
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Study Characteristics All nine included studies were designed to compare TC with usual physical activities, involving a total of 632 healthy adults. All except two studies22,23 focused on middle-aged and older adults with ages ranging from 45 to 79 years. Six studies17,21–25 were conducted in China, one18 in Vietnam, and two19,20 in the U.S. In the included studies, TC intervention varied widely in practice frequency, duration, and style. The duration of TC practice ranged from 6 weeks to 3 years, and the frequency varied from one to seven sessions per week and 30 to 90 minutes per session. The specific style of TC was not provided in four studies,17,18,21,23 whereas the five other studies reported that 12-form Yang style,19 12-form Sun style,20,25 24-form simplified TC,22 or 108-form TC24 was applied. Outcomes from six cognitive domains, which included global cognitive ability, attention, learning and memory, language, emotion and perception, and execution, were assessed using the Mini-Mental State Examination (MMSE),20 Category Verbal Fluency Test (CVFT),19 Clock Drawing Test (CDT),17 Trail Making Test (TMT),18 Stroop Test (ST),22 Mattis Dementia Rating Scale (MDRS),17 and response time.21 The characteristics of the included articles are summarized in Table 1.
Risk of Bias in Included Studies The methodologic quality of the included studies is detailed in Appendix Table 3 (available online). Of the CDFD n=50
CMFD n=75
CPCD n=77
VIP n=10
nine included studies, four reported “random allocation among participants,” but none described the randomization procedures and allocation concealment of the randomization sequence. Only one study20 reported assessor blinding. Intention-to-treat analysis was performed in one study.17 Only one study17 reported loss to follow-up or study withdrawal and clearly described the method of data collection. Therefore, these studies could not be judged to be free of bias from incomplete outcome data. Although the study protocol was not available in all included studies, it was clear that the outcomes listed in the Methods section of each article could be compared with the reported results; therefore, these studies were judged to be at low risk of bias from selective reporting of outcomes. We judged one study25 as “unclear” in terms of freedom from other bias because there was no evidence of statistical testing of baseline characteristics between the comparison groups. Overall, all studies were judged to have a high risk of bias with low methodological quality.
Measures of Effect Global Cognitive Ability Two studies reported on global cognitive ability assessed using MDRS17 or event-related potential 300 (P300).23 We did not meta-analyze these two studies together because of the diversity of outcome measures. However, their separate results showed that TC resulted in an obvious improvement SCI n=103
Embase n=92
Pubmed n=69
Cochrane n=151
97 articles excluded because of reduplication, according to title and author names.
Screening
Potential eligible articles, n=25.
Eligibility
Potentially relevant articles, n=553.
Full-text articles for more detailed evaluation, n=26.
Included
Identification
Wanfang n=23
91
Eligible articles, n=9.
Excluded based on title and abstract, n=528: narrative reviews, n=68; irrelevant to Tai Chi, n=274; irrelevant to cognition, n=153; investigation, n=7; comments, n=22; animal experiments, n=4. 1 article identified from scanning reference of relevant narrative. 17 full-text articles excluded: duplicate publication, n=1; participants were not health adults, n=6; Tai Chi plus other interventions, n=1; no usual physical activity control group, n=4; self controlled trial, n=1; unacceptable cognitive outcomes, n=4.
Included quantitative synthesis, n=6.
Figure 1. Literature search and selection flow diagram showing reasons for exclusion. CDFD, China Doctor Dissertation Full-Text Database; CMFD, Chinese Master’s Theses Full-Text Databases; CPCD, China Proceedings of Conference Full-text Database; SCI, Science Citation Index; VIP, Chinese Scientific Journal Database.
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Table 1. Literature Characteristics Author/ year/ Country
Compare Study design
Sample (I/C)
Mortimer (2012),17 China
RCT
30/30
Nguyen (2012),18 Vietnam
RCT
Taylor (2010),19 America
Participants (age/ years, sex)
Tai Chi/ duration
Outcomes/ measurements
UPA
50 minutes 3 times/ week40 weeks
Global cognition: MDRS Memory: WAISDS, CVFT, AVLT Execution: TMT, CDT, ST
TC (no specific)
UPA
60 minutes 2 times/ week24 weeks
Execution: TMT
Age range: 460 years Sex: male29, female 64;
TC (12-form Yang)
UPA
45 minutes 7 times/ week24 weeks
Memory: WAISDS, CVFT
28/27
Age range: 460 years
TC (12-form Sun)
UPA
40 minutes 3 times/ week20 weeks
Global cognition: MMSE
NRCT
53/48
Age range: 45–74 years Sex: male 49, female 52;
TC (no specific)
UPA
424 weeks
Attention: response time, HFAM, Emotion: arm stability Perception: mental rotation
Liu (2011),22 China
NRCT
31/23
Sex: male 16, female 38
TC (24-form simplified)
UPA
45 minutes 1 time/ week16 weeks
Execution: ST
Lan (2009),23 China
NRCT
17/30
Age: T: 21.33⫾1.75 years; C: 21.23⫾1.52 years
TC (no specific)
UPA
55 minutes 3 times/ week6 weeks
Global cognition: P300
Man (2010),24 China
NRCT
42/44
Age range: 460 years
TC (Ng style)
UPA
45 minutes 3 times/ week3 years
Attention: CTT Memory: RBMT, HKLLT
Wei (2013),25 China
NRCT
22/18
Age: 52⫾6 years
TC (Yang, Wu, Sun, Chen)
UPA
30–90 minutes 7 times/ week14 years
Global cognition: MRI Execution: ANT
Intervention
Control
Age range: 60–70 years Sex: male 20, female 40
TC (no specific)
48/48
Age range: 60–79 years Sex: male 48, female 48
RCT
37/56
Tsai (2013),20 America
RCT
Zhang (2006),21 China
AVLT, Auditory Verbal Learning Test; ANT, Attention Network Test; C, control group; CDT, Clock Drawing Test; CTT, Color Trail Test; CVFT, Category Verbal Fluency Test; HFAM, hands and feet alternating movement; HKLLT, Hong Kong List Learning Test; I, intervention group; MDRS, Mattis Dementia Rating Scale; MRI, magnetic resonance imaging; MMSE, Mini-Mental State Examination; NR, not reported; NRCT, non-randomized controlled trial; RBMT, Rivermead Behavioral Memory Test; ST, Stroop Test; P300, event-related potential 300; TC, Tai Chi; TMT-A, Trail Making Test Part A; TMT-B, Trail Making Test Part B; UPA, usual physical activity; WAIS-DS, Wechsler Adult Intelligence Scale–Digit Span.
in MDRS scores (MD¼4.59, 95% CI¼1.37, 7.81, p¼0.005) and a reduction in P300 reaction time (MD¼–33.08, 95% CI¼–55.99, –10.17, p¼0.005) and P300 latency period (MD¼–20.54, 95% CI¼–39.15, –1.93, p¼0.03) compared with the usual physical activities (Table 2). One study20 reported that TC training participants had higher MMSE scores than those in the usual physical activities group, but the difference was not significant (p¼0.096).
Attention Attention was reported in three studies17,21,24 comparing TC exercise with the usual physical activities. One
study17 reported the significant improvement in MDRS attention score following TC exercise (MD¼0.52, 95% CI¼0.08, 0.96, p¼0.02). One study21 reported that TC resulted in an obvious improvement of attention focus time (MD¼1.48, 95% CI¼1.06, 1.90, po0.0001); time of correct hands and feet alternating movement (HFAM; MD¼15.62, 95% CI¼8.91, 22.33, po0.00001); and mean HFAM time (MD¼14.56, 95% CI¼8.10, 21.02, po0.00001) as well as a clear decrease in attention dispersal time (MD¼–7.68, 95% CI¼–9.63, –5.37, po0.0001); mean response time (MD¼–136.19, 95% CI¼–198.81, –73.57, po0.0001); and total HFAM time
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Table 2. Tai Chi Exercise on Global Cognitive Ability Compared With Usual Physical Activity
Measure MDRS score
No. of studies
No. of participants
1: Mortimer (2012)17
MD (95% CI)
60 (I: 30; C: 30)
4.59 (1.37, 7.81)
Test for overall effect (p-value) 0.005
P300 response time (ms)
1: Lan (2009)
23
47 (I: 17; C: 30)
–33.1 (–55.99, –10.17)
0.005
P300 latency period (ms)
1: Lan (2009)23
47 (I: 17; C: 30)
–20.5 (–39.15, –1.93)
0.03
P300 wave amplitude
1: Lan (2009)23
47 (I: 17; C: 30)
0.17 (–1.46, 1.80)
0.84
Note: Boldface indicates statistical significance (po0.05). C, control group; I, intervention group; MDRS, Mattis Dementia Rating Scale; ms, milliseconds; MD, mean difference.
(MD¼–209.03, 95% CI¼–325.34, –65.72, p¼0.004). However, no significant changes were found for optimal response time in the study (Table 3). Another study24 also reported a significantly positive effect of TC exercise on attention, which was evaluated by the Color Trail Test (A-1 and 2) (po0.01; no available data were extracted).
However, another study24 reported that the TC group had better memory ability performance than the usual physical activities control group as assessed by the Rivermead Behavioral Memory Test (RBMT-CV) and Hong Kong List Learning Test (HKLLT) (po0.01; no available data were extracted).
Learning and Memory
Emotion and Perception
Comparing with the usual physical activities, TC exercise significantly improved the level of learning and memory as assessed by MDRS memory score (one trial,17 MD¼1.01, 95% CI¼0.02, 2.0, p¼0.05); Wechsler Adult Intelligence Scale–Digit Span (WAIS-DS; forward) (two trials,17,19 MD=–0.46, 95% CI=–0.89, –0.03, p=0.04); and Auditory Verbal Learning Test (AVLT; delayed recognition) (one trial,17 MD¼2.01, 95% CI¼0.37, p¼0.02). Other measurements, including CVFT, WAISDS (backward), and AVLT (immediate recall), were not shown to have a significant difference (Table 4).
One trial21 with 93 participants reported on emotion and perception ability as assessed by measuring arm stability and mental rotation time. Compared with the usual physical activities, TC exercise significantly improved arm stability (MD¼3.71, 95% CI¼0.86, 6.56, p¼0.01) and mental rotation time (MD¼–0.39, 95% CI¼–0.77, –0.01, p¼0.05) (Table 5).
Execution Three trials17,18,22 involving 217 participants reported on execution ability assessed by TMT, ST, and CDT (Table 6). Compared with the usual physical activities, TC exercise
Table 3. Tai Chi Exercise on Attention Compared With Usual Physical Activity
Measure
No. of studies
No. of participants
MD (95% CI)
Test for overall effect (p-value)
Time of attention focus (seconds)
1: Zhang (2006)21
93 (I: 50; C: 43)
1.48 (1.06, 1.90)
o0.00001
No. of times attention dispersed (M)
1: Zhang (2006)21
93 (I: 50; C: 43)
–7.68 (–9.63, –5.37)
o0.00001
Response time (seconds; M)
1: Zhang (2006)21
93 (I: 50; C: 43)
–136.19 (–198.81, –73.57)
o0.0001
Optimal response time (seconds)
21
1: Zhang (2006)
93 (I: 50; C: 43)
Total time of HFAM (seconds)
1: Zhang (2006)21
93 (I: 50; C: 43)
No. of times HFAM done correctly (M)
1: Zhang (2006)21
93 (I: 50; C: 43)
15.62 (8.91, 22.33)
o0.00001
Mean time of HFAM (seconds)
1: Zhang (2006)21
93 (I: 50; C: 43)
14.56 (8.10, 21.02)
o0.00001
60 (I: 30; C: 30)
0.52 (0.08, 0.96)
0.02
MDRS attention score (M)
17
1: Mortimer (2012)
–31.17 (–67.78, 5.44) –209.03 (–325.34, –65.72)
0.10 0.004
Note: Boldface indicates statistical significance (po0.05). C, control group; HFAM, hands and feet alternating movement; I, intervention group; MD, mean difference; MDRS, Mattis Dementia Rating Scale.
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Table 4. Tai Chi Exercise on Learning and Memory Compared With Usual Physical Activity Heterogeneity Measure (score)
No. of studies
No. of participants
MD (95% CI)
I²
p-value
Test for overall effect (p-value)
MDRS memory score
1: Mortimer (2012)17
60 (I: 30; C: 30)
1.01 (0.02, 2.0)
—
—
0.05
CVFT, animals
2: Mortimer (2012),17 Taylor (2010)19
153 (I: 67; C: 86)
–1.13 (–2.47, 0.21)
84%
0.01
0.10
WAIS-DS, forward
2: Mortimer (2012),17 Taylor (2010)19
153 (I: 67; C: 86)
–0.46 (–0.89, –0.03)
71%
0.07
0.04
WAIS-DS, backward
2: Mortimer (2012),17 Taylor (2010)19
153 (I: 67; C: 86)
0.21 (–0.47, 0.89)
0%
0.75
0.55
AVLT, immediate recall
1: Mortimer (2012)17
60 (I: 30; C: 30)
0.38 (–0.74, 1.5)
—
—
0.51
AVLT, delayed recall
1: Mortimer (2012)17
60 (I: 30; C: 30)
1.22 (–0.4, 2.84)
—
—
0.14
AVLT, delayed recognition
1: Mortimer (2012)17
60 (I: 30; C: 30)
2.01 (0.37, 3.65)
—
—
0.02
Note: Boldface indicates statistical significance (po0.05). AVLT, Auditory Verbal Learning Test; C, control group; CVFT, Category Verbal Fluency Test; DS, Digit Span test; I, intervention group; MD, mean difference; MDRS, Mattis Dementia Rating Scale; WAIS, Wechsler Adult Intelligence Scale.
resulted in a positive improvement on execution ability as measured by TMT-B (two trials,17,18 MD=–16.02, 95% CI=–18.66, –13.37, po0.0001), ST-word (two trials,17,22 MD=–0.46, 95% CI=–0.9, –0.03, p=0.04), and ST-color– word (two trials,17,22 MD=–1.73, 95% CI=–3.42, –0.04, p=0.04). There was, however, no significant change in values of TMT-A, ST-color, and CDT. Another study25 reported improvement in executive ability assessed by the Attention Network Test. In addition, the brain was reshaped through TC exercise, which was associated with greater intensity of TC practice.
Safety and Adverse Events No adverse events were reported in the included studies.
Discussion This systematic review examined the protective effects of TC exercise on the cognitive ability of healthy adults.
Nine studies involving 632 participants were included in this review. All studies were designed to compare TC exercise with usual physical activities. As a whole, the included studies were of low quality. We attempted to contact the original authors by telephone and e-mail for further information. However, most replies were unsatisfactory or had little ability to resolve our questions, and some of the authors did not reply or could not be contacted. Nevertheless, the results of this review showed that TC exercise could significantly improve the majority of outcomes of global cognitive ability, attention, learning and memory, language, emotion and perception, and execution in healthy adults. It may, therefore, be helpful in protecting the cognitive ability of healthy adults. The benefits of exercise on cognitive ability have been widely recognized. Studies have shown that people who were more active in midlife and late life have a lower risk of global cognitive decline.26,27 People who walk more than two miles per day have a significantly lower risk of
Table 5. Tai Chi Exercise on Emotion and Perception Compared With Usual Physical Activity
Measure Emotion: Arm stability (score) Perception: Mental rotation (score)
No. of studies
No. of participants
MD (95% CI)
Test for overall effect (p-value)
1: Zhang (2006)21
93 (I: 50; C: 43)
3.71 (0.86, 6.56)
0.01
21
93 (I: 50; C: 43)
–0.39 (–0.77, –0.01)
0.05
1: Zhang (2006)
Note: Boldface indicates statistical significance (po0.05). C, control group; I, intervention group; MD, mean difference.
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95
Table 6. Tai Chi Exercise on Execution Compared With Usual Physical Activity Heterogeneity Measure (score)
No. of studies
No. of participants
MD (95% CI)
I²
p-value
Test for overall effect (p-value)
TMT-A
2: Nguyen (2012),18 Mortimer (2012)17
133 (I: 69; C: 64)
6.88 (–1.74, 15.50)
0%
0.84
TMT-B
2: Nguyen (2012),18 Mortimer (2012)17
133 (I: 69; C: 64)
–16.02 (–18.66, –13.37)
81%
0.02
ST-word (CWT-A)
2: Liu (2011),22 Mortimer (2012)17
144 (I: 61; C: 53)
–0.46 (–0.90, –0.03)
48%
0.16
0.04
ST-color (CWT-B)
2: Liu (2011),22 Mortimer (2012)17
144 (I: 61; C: 53)
–0.02 (–0.89, 0.84)
0%
0.48
0.96
ST-color–word (CWT-C)
2: Liu (2011),22 Mortimer (2012)17
144 (I: 61; C: 53)
–1.73 (–3.42, –0.04)
58%
0.12
0.04
CDT
1: Mortimer (2012)17
60 (I: 30; C: 30)
–0.62 (–2.79, 1.55)
—
—
0.58
0.12 o0.00001
Note: Boldface indicates statistical significance (po0.05). C, control group; CDT, Clock Drawing Test; I, intervention group; ST, Stroop Test; TMT-A, Trail Making Test Part A; TMT-B, Trail Making Test Part B; MD, mean difference.
developing dementia compared with those who walk less than one mile per day.28 TC is a traditional Chinese exercise that has been developed since the 17th century. During the process of development, TC was differentiated into five main styles: Chen, Yang, Wu, Sun, and simplified TC. In recent years, TC has become a popular exercise worldwide, and research on its benefits is flourishing. However, the majority of these studies have focused on the effects of TC on muscular strength,29 balance,30 the vestibular system,31 prevention of falls,32 physical function,33 and quality of life.34 Currently, a limited number of studies have assessed the use of TC to preserve the cognitive ability of older adults. As a form of physical exercise, TC is a light to moderate– intensity aerobic activity with estimated METs between 1.5 and 4.0.35,36 Its exercise intensity can be easily adjusted by controlling the speed and postural height. Theoretically, aerobic exercise could promote cognitive ability by directly improving the cerebral circulation and the action of neurotransmitters. In addition, as a mind–body exercise, TC involves learning and memorization of new skills and movement patterns, and sustaining attention focus, which could be helpful to train working memory, divided attention, cognitive flexibility, and overall executive ability. Two previous reviews systematically assessed the effect of TC on cognitive ability in an older population with or without cognitive impairment and suggested small to moderate improvements in executive ability, language, learning, and memory. However, the interventions in the control groups were diverse in their included studies, in which other exercises, handicrafts, education and social activities, rehabilitation, and other interventions were July 2015
applied.37,38 Therefore, the protective efficacy of TC compared to the usual physical activities for maintaining cognitive ability among healthy adults remains ambiguous. The present review was designed to assess the efficacy of TC exercise on the cognitive ability by comparison with the usual physical activities. Although only nine eligible studies were included in this review, pooled analyses were not performed, owing to use of different outcomes and variability in the amount of exercise, number of participants, and methodological quality among the included studies. TC in these studies showed a positive association with the majority of outcomes of global cognitive ability, attention, learning and memory, language, emotion and perception, and execution among healthy adults.
Limitations and Recommendations for Future Research This study had several limitations. First, the number of studies and the clinical heterogeneity of the outcomes made their synthesis and meta-analysis difficult, and publication bias was not explored by funnel plot analysis because of an insufficient number of included studies.39 Second, the overall methodological quality of the included studies was low. If more definitive conclusions are to be drawn, large-scale and high-quality RCTs should be encouraged. Third, subjective assessments were used in most studies. In order to better evaluate the effects of TC exercise on cognitive ability, future studies should make use of various objective detection methods and instruments (e.g., event-related potential, functional magnetic resonance imaging). In addition, the
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Type I error was likely inflated given great differences in the design and outcomes reported among different studies, whereas significant results were observed only in one or two studies. Finally, limitations were also seen in the lack of TC standardization, with variations in the intensity of each session, styles, and teaching quality. Standardized TC exercise is useful in ensuring good homogeneity and demonstrating its effectiveness. Therefore, future studies should not only report important design features (e.g., blinding, randomization) but also illustrate the features relevant to TC specifically.
Conclusions In order to make more definitive conclusions regarding the potential protective effects of TC on the cognitive ability of healthy adults, more rigorously designed, largescale RCTs are required in future research. The authors thank Dr. Li Ge (School of Nursing, Fujian University of Traditional Chinese Medicine) for her helpful evaluation and revision of the second revised manuscript. This systematic review is supported by the Collaboration Innovation Center for Rehabilitation Technology (Number 1 Collaboration Center [2012]) and the Rehabilitation Research Center for Traditional Chinese Medicine, State Administration of Traditional Chinese Medicine of the People’s Republic of China. ZGH, TJ, and CLD conceived of the study, LFW drafted the manuscript, and ZGH revised it and wrote several sections of this manuscript. LSZ and HMM were the research assistants who helped with data extraction, quality assessment, and other aspects of the study. All authors contributed to the writing of the manuscript and have read and approved the final version for publication. ZGH and LFW contributed equally to this study. No financial disclosures were reported by the authors of this paper.
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Appendix Supplementary data Supplementary data associated with this article can be found at http://dx.doi.org/10.1016/j.amepre.2015.01.002.
