Impact of Short- and Long-term Tai Chi Mind-Body Exercise Training on Cognitive Function in Healthy Adults: Results From a Hybrid Observational Study and Randomized Trial

Jacquelyn N Walsh, Brad Manor, Jeffrey Hausdorff, Vera Novak, Lewis Lipsitz, Brian Gow, Eric A Macklin, Chung-Kang Peng, Peter M Wayne, Jacquelyn N Walsh, Brad Manor, Jeffrey Hausdorff, Vera Novak, Lewis Lipsitz, Brian Gow, Eric A Macklin, Chung-Kang Peng, Peter M Wayne

Abstract

Background: Cognitive decline amongst older adults is a significant public health concern. There is growing interest in behavioral interventions, including exercise, for improving cognition. Studies to date suggest tai chi (TC) may be a safe and potentially effective exercise for preserving cognitive function with aging; however, its short-term and potential long-term impact on physically active, healthy adults is unclear.

Objective: To compare differences in cognitive function among long-term TC expert practitioners and age-matched and gender-matched TC-naïve adults and to determine the effects of short-term TC training on measures of cognitive function in healthy, nonsedentary adults.

Design: A hybrid design including an observational comparison and a 2-arm randomized clinical trial (RCT).

Participants: Healthy, nonsedentary, TC-naive adults (50 y-79 y) and age-matched and gender-matched long-term TC experts.

Methods: A cross-sectional comparison of cognitive function in healthy TC-naïve (n=60) and TC expert (24.5 y ÷ 12 y experience; n=27) adults: TC-naïve adults then completed a 6-month, 2-arm, wait-list randomized clinical trial of TC training. Six measures of cognitive function were assessed for both cross-sectional and longitudinal comparisons.

Results: TC experts exhibited trends towards better scores on all cognitive measures, significantly so for category fluency (P=.01), as well as a composite z score summarizing all 6 cognitive assessments (P=.03). In contrast, random assignment to 6 months of TC training in TC-naïve adults did not significantly improve any measures of cognitive function.

Conclusions: In healthy nonsedentary adults, long-term TC training may help preserve cognitive function; however, the effect of short-term TC training in healthy adults remains unclear.

Trial registration: ClinicalTrials.gov NCT01340365.

Keywords: Aging; cognitive function; dementia; tai chi.

Figures

Figure 1
Figure 1
CONSORT Flow
Figure 2
Figure 2
Comparisons of cognitive performance between tai chi (TC) expert and TC-naïve adults. Symbols represent group means along with standard errors. Means were estimated using linear models controlling for education, age, gender, body mass index, and physical activity level (*P<.01). TC experts had significantly higher net cognitive function based on a composite z score calculated as the sum of z scores from all 6 cognitive outcomes (P=.028; see Table 2). Abbreviations: DS LONGESTBKWD, Digit Span longest backward span; DS LONGESTFWD, Digit Span longest forward Span; TC, tai chi; TMTA, Trail Making Test Part A; TMTB, Trail Making Test Part B. "FAS" represents letter fluency; "FAS_CATEGORY" represents category fluency.

References

    1. Plassman BL, Langa KM, Fisher GG, et al. Prevalence of dementia in the United States: the aging, demographics, and memory study. Neuroepidemiology. 2007;29(1-2):125–32.
    1. Wimo A, Winblad B, Jönsson L. The worldwide societal costs of dementia: Estimates for 2009. Alzheimers Dement. 2010;6(2):98–103.
    1. Hurd MD, Martorell P, Delavande A, Mullen KJ, Langa KM. Monetary costs of dementia in the United States. N Engl J Med. 2013;368(14):1326–34.
    1. Belsky DW, Caspi A, Israel S, Blumenthal JA, Poulton R, Moffitt TE. Cardiorespiratory fitness and cognitive function in midlife: neuroprotection or neuroselection? Ann Neurol. 2015;77(4):607–17.
    1. Lee PL. Cognitive function in midlife and beyond: physical and cognitive activity related to episodic memory and executive functions. Int J Aging Hum Dev. 2015;79(4):263–78.
    1. Kelly ME, Loughrey D, Lawlor BA, Robertson IH, Walsh C, Brennan S. The impact of exercise on the cognitive functioning of healthy older adults: a systematic review and meta-analysis. Ageing Res Rev. 2014. July;16:12–31.
    1. Burgener SC, Yang Y, Gilbert R, Marsh-Yant S. The effects of a multimodal intervention on outcomes of persons with early-stage dementia. Am J Alzheimers Dis Other Demen. 2008;23(4):382–94.
    1. Wayne PM, Fuerst ML. The Harvard Medical School guide to tai chi. Boston: Shambhala Publications, Inc; 2013.
    1. Yeh GY, Wang C, Wayne PM, Phillips R. Tai chi exercise for patients with cardiovascular conditions and risk factors: A systematic review. J Cardiopulm Rehabil Prev. 2009;29(3):1521–60.
    1. Logghe IH, Verhagen AP, Rademaker AC, et al. The effects of Tai Chi on fall prevention, fear of falling and balance in older people: A meta-analysis. Prev Med. 2010;51(3/4):222–7.
    1. Wang C, Bannuru R, Ramel J, et al. Kupelnick B, Scott T, Schmid CH. Tai Chi on psychological well-being: systematic review and meta-analysis. BMC Complement Altern Med. 2010. May 21;10:23.
    1. Wayne PM, Berkowitz DL, Litrownik DE, Buring JE, Yeh GY. What do we really know about the safety of tai chi?: A systematic review of adverse event reports in randomized trials. Arch Phys Med Rehabil. 2014;95(12):2470–83.
    1. Wayne PM, Walsh JN, Taylor-Piliae RE, et al. Effect of tai chi on cognitive performance in older adults: systematic review and meta-analysis. J Am Geriatr Soc. 2014;62(1):25–39.
    1. Li R, Zhu X, Yin S, et al. Multimodal intervention in older adults improves resting-state functional connectivity between the medial prefrontal cortex and medial temporal lobe. Front Aging Neurosci. 2014 Mar 10;6:39.
    1. Mortimer JA, Ding D, Borenstein AR, et al. Changes in brain volume and cognition in a randomized trial of exercise and social interaction in a community-based sample of non-demented Chinese elders. J Alzheimers Dis. 2012;30(4):757–66.
    1. Wei GX, Xu T, Fan FM, et al. Can Taichi reshape the brain? A brain morphometry study. PloS One. 2013;8(4):e61038.
    1. Deschamps A, Onifade C, Decamps A, Bourdel-Marchasson I. Health-related quality of life in frail institutionalized elderly: effects of a cognition-action intervention and Tai Chi. J Aging Phys Act. 2009;17(2):236–48.
    1. Lam LC, Chau RC, Wong BM, et al. Interim follow-up of a randomized controlled trial comparing Chinese style mind body (Tai Chi) and stretching exercises on cognitive function in subjects at risk of progressive cognitive decline. Int J Geriatr Psychiatry. 2011;26(7):733–40.
    1. Lavretsky H, Alstein LL, Olmstead RE, et al. Complementary use of tai chi chih augments escitalopram treatment of geriatric depression: a randomized controlled trial. Am J Geriatr Psychiatry. 2011;19(10):839–50.
    1. Reid-Arndt SA, Matsuda S, Cox CR. Tai Chi effects on neuropsychological, emotional, and physical functioning following cancer treatment: a pilot study. Complement Ther Clin Pract. 2012;18(1):26–30.
    1. Wayne PM, Gow BJ, Costa MD, et al. Complexity-based measures inform effects of tai chi training on standing postural control: cross-sectional and randomized trial studies. PLoS One. 2014;9(12):e114731.
    1. Wayne PM, Hausdorff JM, Lough M, et al. Tai Chi training reduces dual task gait variability, a potential mediator of fall risk, in healthy older adults: cross-sectional and randomized trial studies. Front Hum Neurosci. Neuroscience 2015; In press.
    1. Wayne PM, Manor B, Novak V, et al. A systems biology approach to studying Tai Chi, physiological complexity and healthy aging: design and rationale of a pragmatic randomized controlled trial. Contemp Clin Trials. 2013;34(1):21–34.
    1. Fischer M, Fugate-Woods N, Wayne PM. Use of pragmatic community-based interventions to enhance recruitment and adherence in a randomized trial of Tai Chi for women with osteopenia: insights from a qualitative substudy. Menopause. 2014;21(11):1181–9.
    1. Bowie CR, Harvey PD. Administration and interpretation of the Trail Making Test. Nat Protoc. 2006;1(5):2277–81.
    1. Strauss E, Sherman E, Spreen O. A compendium of neuropsychological tests. 3rd ed New York: Oxford University Press, Inc.; 2006.
    1. Reitan R. Validity of the Trail Making Test as an indicator of organic brain damage. : Goldstein G, Beers SR, editors Comprehensive handbook of psychological assessment, intellectual and neuropsychological assessment: John Wiley & Sons, Ltd; 1958: 271–6.
    1. Blankenship AB. Memory span: a review of the literature. Psychol Bull. 1938;35(1):1–25
    1. Benton AL, Sivam AB, Hamsher Kd, Varney N, Spreen O. Contributions to neuropsychological assessment: a clinical mannual. New York: Oxford University Press; 1983.
    1. Arbuthnott K, Frank J. Trail making test, part B as a measure of executive control: validation using a set-switching paradigm. J Clin Exp Neuropsychol. 2000;22(4):518–28.
    1. Franzen M. Cross-validation of the alternative forms of reliability of the Trailmaking Test. Arch Clin Neuropsychol. 1996;11(5):390–1.
    1. Ross TP, Calhoun E, Cox T, Wenner C, Kono W, Pleasant M. The reliability and validity of qualitative scores for the Controlled Oral Word Association Test. Arch Clin Neuropsychol. 2007;22(4):475–88.
    1. Ross TP, Furr AE, Carter SE, Weinberg M. The psychometric equivalence of two alternate forms of the Controlled Oral Word Association Test. Clin Neuropsychol. 2006;20(3):414–31.
    1. Angevaren M, Aufdemkampe G, Verhaar HJ, Aleman A, Vanhees L. Physical activity and enhanced fitness to improve cognitive function in older people without known cognitive impairment. Cochrane Database Syst Rev. 2008. July 16(3):CD005381.
    1. Brown AK, Liu-Ambrose T, Tate R, Lord SR. The effect of group-based exercise on cognitive performance and mood in seniors residing in intermediate care and self-care retirement facilities: a randomised controlled trial. Br J Sports Med. 2009;43(8):608–14.
    1. Baumgartner T, Jackson A, Mahar M, Rowe D. (2006) Measurement for evaluation in physical education and exercise science. New York: McGraw-Hill; 2006.
    1. Heil DP, Freedson PS, Ahlquist LE, Price J, Rippe JM. Nonexercise regression models to estimate peak oxygen consumption. Med Sci Sports Exer. 1995;27(4):599–606.
    1. Ware JE, Kosinski M. Interpreting SF-36 summary health measures: a response. Qual Life Res. 2001;10(5):405–13; discussion 415-20.
    1. Ware JE, Sherbourne CD. The MOS 36-item short-form health survey (SF-36): I. Conceptual framework and item selection. Med Care. 1992;30:473–83.
    1. Liang KY, Zeger SL. Longitudinal data analysis of continuous and discrete responses for pre-post designs. Indian J Stat (Series B). 2000;62(1):134–48.
    1. Man DW, Tsang WW, Hui-Chan CW. Do older t'ai chi practitioners have better attention and memory function? J Altern Complement Med. 2010;16(12):1259–64.
    1. Lam LC, Tam CW, Lui VW, et al. Modality of physical exercise and cognitive function in Hong Kong older Chinese community. Int J Geriatr Psychiatry. 2009;24(1):48–53.
    1. Chan AS, Ho YC, Cheung MC, Albert MS, Chiu HF, Lam LC. Association between mind-body and cardiovascular exercises and memory in older adults. J Am Geriatr Soc. 2005;53(10):1754–60.
    1. Lu X, Siu KC, Fu SN, Hui-Chan CW, Tsang WW. Tai Chi practitioners have better postural control and selective attention in stepping down with and without a concurrent auditory response task. Eur J Appl Physiol. 2013;113(8):1939–45.
    1. Cheng ST, Chow PK, Song YQ, et al. Mental and physical activities delay cognitive decline in older persons with dementia. Am J Geriatr Psychiatry. 2014;22(1):63–74.
    1. Lam LC, Chau RC, Wong BM, et al. A 1-year randomized controlled trial comparing mind body exercise (Tai Chi) with stretching and toning exercise on cognitive function in older Chinese adults at risk of cognitive decline. J Am Med Dir Assoc. 2012;13(6):568.
    1. Nguyen MH, Kruse A. A randomized controlled trial of Tai chi for balance, sleep quality and cognitive performance in elderly Vietnamese. Clin Interv Aging. 2012;7:185–90.
    1. Taylor-Piliae RE, Newell KA, Cherin R, Lee MJ, King AC, Haskell WL. Effects of Tai Chi and Western exercise on physical and cognitive functioning in healthy community-dwelling older adults. J Aging Phys Act. 2010;18(3):261–79.
    1. Tsai PF, Chang JY, Beck C, Kuo YF, Keefe FJ. A pilot cluster-randomized trial of a 20-week Tai Chi program in elders with cognitive impairment and osteoarthritic knee: effects on pain and other health outcomes. J Pain Symptom Manage. 2012;45(4):660–9.
    1. Dechamps A, Diolez P, Thiaudière E, et al. Effects of exercise programs to prevent decline in health-related quality of life in highly deconditioned institutionalized elderly persons: a randomized controlled trial. Arch Intern Med. 2010;170(2):162–9.
    1. Wang W, Sawada M, Noriyama Y, et al. Tai Chi exercise versus rehabilitation for the elderly with cerebral vascular disorder: a single-blinded randomized controlled trial. Psychogeriatrics. 2010;10(3):160–6.
    1. Crum RM, Anthony JC, Bassett SS, Folstein MF. Population-based norms for the Mini-Mental State Examination by age and educational level. JAMA. 1993;269(18):2386–91.
    1. Hester RL, Kinsella GJ, Ong B. Effect of age on forward and backward span tasks. J Int Neuropsychol Soc. 2004;10(4):475–81.
    1. Tombaugh TN. Trail Making Test A and B: normative data stratified by age and education. Arch Clin Neuropsychol. 2004;19(2):203–14.
    1. Tombaugh TN, Kozak J, Rees L. Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. Arch Clin Neuropsychol. 1999;14(2):167–77.
    1. Fang ZH, Lee CH, Seo MK. et al. Effect of treadmill exercise on the BDNF-mediated pathway in the hippocampus of stressed rats. Neurosci Res. 2013;76(4):187–94.
    1. Erickson KI, Voss MW, Prakash RS, et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A. 2011;108(7):3017–22.
    1. Colcombe SJ, Erickson KI, Scalf PE, et al. Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci. 2006;61(11):1166–70.
    1. Pereira AC, Huddleston DE, Brickman AM, et al. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci U S A. 2007;104(13):5638–43.
    1. Voss MW, Prakash RS, Erickson KI, et al. Plasticity of brain networks in a randomized intervention trial of exercise training in older adults. Front Aging Neurosci. 2010. August 26;2.
    1. Voelcker-Rehage C, Godde B, Staudinger UM. Cardiovascular and coordination training differentially improve cognitive performance and neural processing in older adults. Front Hum Neurosci. 2011. March 17;5:26.
    1. Driemeyer J, Boyke J, Gaser C, Büchel C, May A. Changes in gray matter induced by learning—revisited. PloS One. 2008;3(7):e2669.
    1. Herdener M, Esposito F, di Salle F, et al. Musical training induces functional plasticity in human hippocampus. J Neurosci. 2010;30(4):1377–84.
    1. Hufner K, Binetti C, Hamilton DA, et al. Structural and functional plasticity of the hippocampal formation in professional dancers and slackliners. Hippocampus. 2011;21(8):855–65.
    1. Kattenstroth JC, Kolankowska I, Kalisch T, Dinse HR. Superior sensory, motor, and cognitive performance in elderly individuals with multi-year dancing activities. Front Aging Neurosci. 2010. July 21;2:31.
    1. Tsang WW, Kwok JC, Hui-Chan CW. Effects of aging and tai chi on a finger-pointing task with a choice paradigm. Evid Based Complementary Alternat Med. 2013;2013:653437.
    1. Lupien SJ, de Leon M, de Santi S, et al. Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nature Neurosci. 1998;1(1):69–73.
    1. Fischer M, Fugate-Woods N, Wayne PM. Use of pragmatic community-based interventions to enhance recruitment and adherence in a randomized trial of Tai Chi for women with osteopenia: insights from a qualitative substudy. Menopause. 2014;21(11):1181–9.
    1. Yang Y, Decelle S, Reed M, Rosengren K, Schlagal R, Greene J. Subjective experiences of older adults practicing taiji and qigong. J Aging Res. 2011;2011:650210.
    1. Verghese J, Lipton RB, Katz MJ, et al. Leisure activities and the risk of dementia in the elderly. N Engl J Med. 2003;348(25):2508–16.
    1. Fratiglioni L, Wang H-X, Ericsson K, Maytan M, Winblad B. Influence of social network on occurrence of dementia: a community-based longitudinal study. Lancet. 2000;355(9212):1315–19.

Source: PubMed

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