Tai Chi training's effect on lower extremity muscle co-contraction during single- and dual-task gait: Cross-sectional and randomized trial studies

Peter M Wayne, Brian J Gow, Fengzhen Hou, Yan Ma, Jeffrey M Hausdorff, Justine Lo, Pamela M Rist, Chung-Kang Peng, Lewis A Lipsitz, Vera Novak, Brad Manor, Peter M Wayne, Brian J Gow, Fengzhen Hou, Yan Ma, Jeffrey M Hausdorff, Justine Lo, Pamela M Rist, Chung-Kang Peng, Lewis A Lipsitz, Vera Novak, Brad Manor

Abstract

Background: Tai Chi (TC) mind-body exercise has been shown to reduce falls and improve balance and gait, however, few studies have evaluated the role of lower extremity muscle activation patterns in the observed benefits of TC on mobility.

Purpose: To perform an exploratory analysis of the association between TC training and levels of lower extremity muscle co-contraction in healthy adults during walking under single-task (ST) and cognitive dual-task (DT) conditions.

Methods: Surface electromyography of the anterior tibialis and lateral gastrocnemius muscles was recorded during 90 sec trials of overground ST (walking normally) and DT (walking with verbalized serial subtractions) walking. A mean co-contraction index (CCI), across all strides, was calculated based on the percentage of total muscle activity when antagonist muscles were simultaneously activated. A hybrid study design investigated long-term effects of TC via a cross-sectional comparison of 27 TC experts and 60 age-matched TC-naïve older adults. A longitudinal comparison assessed the shorter-term effects of TC; TC-naïve participants were randomly allocated to either 6 months of TC training or to usual care.

Results: Across all participants at baseline, greater CCI was correlated with slower gait speed under DT (β(95% CI) = -26.1(-48.6, -3.7)) but not ST (β(95% CI) = -15.4(-38.2, 7.4)) walking. Linear models adjusting for age, gender, BMI and other factors that differed at baseline indicated that TC experts exhibited lower CCI compared to TC naives under DT, but not ST conditions (ST: mean difference (95% CI) = -7.1(-15.2, 0.97); DT: mean difference (95% CI) = -10.1(-18.1, -2.4)). No differences were observed in CCI for TC-naive adults randomly assigned to 6 months of TC vs. usual care.

Conclusion: Lower extremity muscle co-contraction may play a role in the observed benefit of longer-term TC training on gait and postural control. Longer-duration and adequately powered randomized trials are needed to evaluate the effect of TC on neuromuscular coordination and its impact on postural control.

Trial registration: The randomized trial component of this study was registered at ClinicalTrials.gov (NCT01340365).

Conflict of interest statement

I have read the journal's policy and the authors of this manuscript have the following competing interests: Peter Wayne is the founder and sole owner of the Tree of Life Tai Chi Center. Peter Wayne's interests were reviewed and managed by the Brigham and Women's Hospital and Partner's HealthCare in accordance with their conflict of interest policies. This does not alter our adherence to PLOS ONE policies on sharing data and materials. No other authors have any potential conflicts to disclose.

Figures

Fig 1. Participant flow through the randomized…
Fig 1. Participant flow through the randomized trial sub-study.
Fig 2. Calculation of lower limb muscle…
Fig 2. Calculation of lower limb muscle co-contraction index.
The EMG signals of the anterior tibialis and lateral gastrocnemius muscles were extracted from each stride of each walking trial, then averaged, and then normalized relative to the mean of the maximum EMG amplitudes for all strides. The common area is the overlapping region under the curves of the EMG signals and represents the muscle co-contraction index. Adapted from Lo et. al. 2017 [29].
Fig 3
Fig 3
Unadjusted associations between co-contraction vs. gait speed and stride time variability (%CV) across all subjects at baseline (solid line). A) Gait speed vs. co-contraction index (CCI) association under the single-task condition, B) gait speed vs. CCI association under the dual-task condition, C) CV vs. CCI association under the single-task condition, D) CV vs. CCI under the dual-task condition.
Fig 4. Co-contraction for age-matched Tai Chi…
Fig 4. Co-contraction for age-matched Tai Chi expert and naïve older adults.
Comparison between naïve and experts with age, gender, BMI, activity, education, hallway length, and executive function Z-score adjusted mean values and standard errors, shown under single-task (ST) and dual-task (DT).

References

    1. Krasovsky T, Levin MF. Review: toward a better understanding of coordination in healthy and poststroke gait. Neurorehabilitation and neural repair. 2010;24(3):213–24. Epub 2009/10/14. 10.1177/1545968309348509 .
    1. Hallal CZ, Marques NR, Spinoso DH, Vieira ER, Gonçalves M. Electromyographic patterns of lower limb muscles during apprehensive gait in younger and older female adults. Journal of Electromyography and Kinesiology. 2013;23:1145–9. 10.1016/j.jelekin.2013.06.006 .
    1. Callisaya ML, Blizzard L, Schmidt MD, McGinley JL, Srikanth VK. Ageing and gait variability—a population-based study of older people. Age and ageing. 2010;39(2):191–7. 10.1093/ageing/afp250
    1. Busse ME, Wiles CM, Van Deursen RWM. Co-activation: Its association with weakness and specific neurological pathology. Journal of NeuroEngineering and Rehabilitation. 2006;3:1–8. 10.1186/1743-0003-3-1 .
    1. Hallal CZ, Marques NR, Vieira ER, Brunt D, Spinoso DH, Castro A, et al. Lower limb muscle coactivation levels in healthy younger and older adults during functional dual-task gait. Motriz Revista de Educacao Fisica. 2013;19:620–6. 10.1590/S1980-65742013000300013 .
    1. Hortobágyi T, Solnik S, Gruber A, Rider P, Steinweg K, Helseth J, et al. Interaction between age and gait velocity in the amplitude and timing of antagonist muscle coactivation. Gait and Posture. 2009;29:558–64. 10.1016/j.gaitpost.2008.12.007 .
    1. Ho CY, Bendrups AP. Ankle reflex stiffness during unperceived perturbation of standing in elderly subjects. The journals of gerontology Series A, Biological sciences and medical sciences. 2002;57:B344–B50. 10.1093/gerona/57.9.b344 .
    1. Peterson DS, Martin PE. Effects of age and walking speed on coactivation and cost of walking in healthy adults. Gait and Posture. 2010;31:355–9. 10.1016/j.gaitpost.2009.12.005 .
    1. Mian OS, Thom JM, Ardigò LP, Narici MV, Minetti AE. Metabolic cost, mechanical work, and efficiency during walking in young and older men. Acta Physiologica. 2006;186:127–39. 10.1111/j.1748-1716.2006.01522.x .
    1. Benjuya N, Melzer I, Kaplanski J. Aging-Induced Shifts From a Reliance on Sensory Input to Muscle Cocontraction During Balanced Standing. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2004;59:M166–M71. 10.1093/gerona/59.2.m166 .
    1. Nagai K, Yamada M, Uemura K, Yamada Y, Ichihashi N, Tsuboyama T. Differences in muscle coactivation during postural control between healthy older and young adults. Archives of Gerontology and Geriatrics. 2011;53(3):338–43. 10.1016/j.archger.2011.01.003
    1. Nagai K, Yamada M, Tanaka B, Uemura K, Mori S, Aoyama T, et al. Effects of balance training on muscle coactivation during postural control in older adults: a randomized controlled trial. Journals of Gerontology Series A: Biomedical Sciences and Medical Sciences. 2012;67(8):882–9.
    1. Freyler K, Weltin E, Gollhofer A, Ritzmann R. Improved postural control in response to a 4-week balance training with partially unloaded bodyweight. Gait & Posture. 2014;40(2):291–6. 10.1016/j.gaitpost.2014.04.186
    1. Wayne PM, Manor B, Novak V, Costa MD, Hausdorff JM, Goldberger AL, et al. A systems biology approach to studying Tai Chi, physiological complexity and healthy aging: design and rationale of a pragmatic randomized controlled trial. Contemporary clinical trials. 2013;34:21–34. 10.1016/j.cct.2012.09.006 .
    1. Wolf SL, Barnhart HX, Ellison GL, Coogler CE. The Effect of Tai Chi Quan and Computerized Balance Training on Postural Stability in Older Subjects. Physical Therapy. 1997;77:371–81. 10.1093/ptj/77.4.371 .
    1. Gillespie LD, Robertson MC, Gillespie WJ, Sherrington C, Gates S, Clemson LM, et al. Interventions for preventing falls in older people living in the community. Cochrane Database of Systematic Reviews. 2012;(9). 10.1002/14651858.CD007146.pub3
    1. Harmer PA, Li F. Tai Chi and falls prevention in older people. Tai Chi Chuan. 52: Karger Publishers; 2008. p. 124–34.
    1. Liu H, Frank A. Tai chi as a balance improvement exercise for older adults: A systematic review. Journal of Geriatric Physical Therapy. 2010;33:103–9. 10.1097/JPT.0b013e3181eda1c4 .
    1. Yan JH. Tai Chi practice improves senior citizens’ balance and arm movement control. Journal of Aging and Physical Activity. 1998;6(3):271–84.
    1. Judge JO, Whipple RH, Wolfson LI. Effects of resistive and balance exercises on isokinetic strength in older persons. Journal of the American Geriatrics Society. 1994;42(9):937–46. 10.1111/j.1532-5415.1994.tb06584.x
    1. Wang C, Collet J, Lau J. The effect of Tai Chi on health outcomes in patients with chronic conditions. ACC Current …. 2004;164:493–501. 10.1001/archinte.164.5.493
    1. Wu G, Zhao F, Zhou X, Wei L. Improvement of isokinetic knee extensor strength and reduction of postural sway in the elderly from long-term Tai Chi exercise. Archives of Physical Medicine and Rehabilitation. 2002;83:1364–9. 10.1053/apmr.2002.34596 .
    1. Judge JO, Lindsey C, Underwood M, Winsemius D. Balance improvements in older women: effects of exercise training. Physical Therapy. 1993;73(4):254–62. 10.1093/ptj/73.4.254
    1. Li F, Harmer P, Fitzgerald K, Eckstrom E, Stock R, Galver J, et al. Tai chi and postural stability in patients with Parkinson's disease. New England Journal of Medicine. 2012;366(6):511–9. 10.1056/NEJMoa1107911
    1. Wayne PM, Hausdorff JM, Lough M, Gow BJ, Lipsitz L, Novak V, et al. Tai Chi Training may Reduce Dual Task Gait Variability, a Potential Mediator of Fall Risk, in Healthy Older Adults: Cross-Sectional and Randomized Trial Studies. Frontiers in Human Neuroscience. 2015;9:1–10. 10.3389/fnhum.2015.00001
    1. Vergara-Diaz G, Osypiuk K, Hausdorff JM, Bonato P, Gow BJ, Miranda JG, et al. Tai Chi for Reducing Dual-task Gait Variability, a Potential Mediator of Fall Risk in Parkinson’s Disease: A Pilot Randomized Controlled Trial. Global Advances In Health and Medicine. 2018;7:2164956118775385 10.1177/2164956118775385
    1. Forrest W. Anticipatory postural adjustment and T'ai Chi Ch'uan. Biomedical sciences instrumentation. 1997;33:65–70.
    1. Gatts SK, Woollacott MH. Neural mechanisms underlying balance improvement with short term Tai Chi training. Aging Clinical and Experimental Research. 2006;18:7–19. 10.1007/BF03324635 .
    1. Lo J, Lo O-Y, Olson EA, Habtemariam D, Iloputaife I, Gagnon MM, et al. Functional implications of muscle co-contraction during gait in advanced age. Gait & Posture. 2017;53:110–4. 10.1016/j.gaitpost.2017.01.010
    1. Wayne PM, Gow BJ, Costa MD, Peng CK, Lipsitz LA, Hausdorff JM, et al. Complexity-based measures inform effects of tai chi training on standing postural control: Cross-sectional and randomized trial studies. PLoS ONE. 2014;9:2005 10.1371/journal.pone.0114731 .
    1. Walsh JN, Manor B, Hausdorff J, Novak V, Lipsitz L, Gow B, et al. 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. Global Advances In Health and Medicine. 2015;4:38–48. 10.7453/gahmj.2015.058 .
    1. Gow BJ, Hausdorff JM, Manor B, Lipsitz LA, Macklin EA, Bonato P, et al. Can Tai Chi training impact fractal stride time dynamics, an index of gait health, in older adults? Cross-sectional and randomized trial studies. PLoS ONE. 2017;12:1–17. 10.1371/journal.pone.0186212 .
    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 osteopenic women: Insights from a qualitative sub-study. Menopause (New York, NY). 2014;21(11):1181.
    1. Arbuthnott K, Frank J. Trail making test, part B as a measure of executive control: validation using a set-switching paradigm. Journal of clinical and experimental neuropsychology. 2000;22(4):518–28. 10.1076/1380-3395(200008)22:4;1-0;FT518
    1. Salthouse TA. Relations between cognitive abilities and measures of executive functioning. Neuropsychology. 2005;19(4):532 10.1037/0894-4105.19.4.532
    1. Zeger SL, Liang K-Y. Longitudinal data analysis for discrete and continuous outcomes. Biometrics. 1986:121–30.
    1. Li JX, Xu DQ, Hong Y. Changes in muscle strength, endurance, and reaction of the lower extremities with Tai Chi intervention. Journal of biomechanics. 2009;42(8):967–71. 10.1016/j.jbiomech.2009.03.001
    1. Xu D-Q, Li J-X, Hong Y. Effect of regular Tai Chi and jogging exercise on neuromuscular reaction in older people. Age and Ageing. 2005;34(5):439–44. 10.1093/ageing/afi114
    1. Fong S-M, Ng GY. The effects on sensorimotor performance and balance with Tai Chi training. Archives of physical medicine and rehabilitation. 2006;87(1):82–7. 10.1016/j.apmr.2005.09.017
    1. Sun W, Zhang C, Song Q, Li W, Cong Y, Chang S, et al. Effect of 1-year regular tai chi on neuromuscular reaction in elderly women: a randomized controlled study. Research in Sports Medicine. 2016;24(2):145–56. 10.1080/15438627.2015.1126280
    1. Wu G. Age-related differences in Tai Chi gait kinematics and leg muscle electromyography: a pilot study. Archives of physical medicine and rehabilitation. 2008;89(2):351–7. 10.1016/j.apmr.2007.08.147
    1. Wu G, Liu W, Hitt J, Millon D. Spatial, temporal and muscle action patterns of Tai Chi gait. Journal of Electromyography and Kinesiology. 2004;14:343–54. 10.1016/j.jelekin.2003.09.002
    1. Tseng SC, Liu W, Finley M, McQuade K. Muscle activation profiles about the knee during Tai-Chi stepping movement compared to the normal gait step. Journal of Electromyography and Kinesiology. 2007;17:372–80. 10.1016/j.jelekin.2005.12.005 .
    1. Wang S-J, Xu D-Q, Li J-X. Effects of regular Tai Chi practice and jogging on neuromuscular reaction during lateral postural control in older people. Research in Sports Medicine. 2017;25(1):111–7. 10.1080/15438627.2016.1258649
    1. Montero‐Odasso M, Verghese J, Beauchet O, Hausdorff JM. Gait and cognition: a complementary approach to understanding brain function and the risk of falling. Journal of the American Geriatrics Society. 2012;60(11):2127–36. 10.1111/j.1532-5415.2012.04209.x
    1. Springer S, Giladi N, Peretz C, Yogev G, Simon ES, Hausdorff JM. Dual‐tasking effects on gait variability: The role of aging, falls, and executive function. Movement disorders: official journal of the Movement Disorder Society. 2006;21(7):950–7.
    1. Sunderaraman P, Maidan I, Kozlovski T, Apa Z, Mirelman A, Hausdorff JM, et al. Differential associations between distinct components of cognitive function and mobility: implications for understanding aging, turning and dual-task walking. Frontiers in aging neuroscience. 2019;11:166 10.3389/fnagi.2019.00166
    1. Wayne PM, Hausdorff JM, Lough M, Gow BJ, Lipsitz L, Novak V, et al. Tai Chi Training may Reduce Dual Task Gait Variability, a Potential Mediator of Fall Risk, in Healthy Older Adults: Cross-Sectional and Randomized Trial Studies. Front Hum Neurosci. 2015;9:332 10.3389/fnhum.2015.00332
    1. Tsang WW, Hui-Chan CW, Fu SN. Effects of Tai Chi on pre-landing muscle response latency during stepping down while performing a concurrent mental task in older adults. Eur J Appl Physiol. 2012;112(7):2663–9. Epub 2011/11/23. 10.1007/s00421-011-2243-2 .
    1. Montero-Odasso M, Verghese J, Beauchet O, Hausdorff JM. Gait and cognition: a complementary approach to understanding brain function and the risk of falling. Journal of the American Geriatrics Society. 2012;60(11):2127–36. 10.1111/j.1532-5415.2012.04209.x
    1. Mirelman A, Gurevich T, Giladi N, Bar‐Shira A, Orr‐Urtreger A, Hausdorff JM. Gait alterations in healthy carriers of the LRRK2 G2019S mutation. Annals of neurology. 2011;69(1):193–7. 10.1002/ana.22165
    1. Mirelman A, Herman T, Brozgol M, Dorfman M, Sprecher E, Schweiger A, et al. Executive function and falls in older adults: new findings from a five-year prospective study link fall risk to cognition. PloS one. 2012;7(6):e40297 10.1371/journal.pone.0040297
    1. Wayne PM, Walsh JN, Taylor‐Piliae RE, Wells RE, Papp KV, Donovan NJ, et al. Effect of Tai Chi on cognitive performance in older adults: Systematic review and meta‐Analysis. Journal of the American Geriatrics Society. 2014;62(1):25–39. 10.1111/jgs.12611
    1. Wu M-T, Tang P-F, Goh JO, Chou T-L, Chang Y-K, Hsu Y-C, et al. Task-Switching Performance Improvements After Tai Chi Chuan Training Are Associated With Greater Prefrontal Activation in Older Adults. Frontiers in aging neuroscience. 2018;10:280 10.3389/fnagi.2018.00280
    1. Jor'dan AJ, Manor B, Hausdorff JM, Lipsitz LA, Habtemariam D, Novak V, et al. Long-term Tai Chi Training Is Associated With Better Dual-task Postural Control and Cognition in Aging Adults. Advances in mind-body medicine. 2018;32(3):4–11.
    1. Ghandali E, Moghadam ST, Hadian MR, Olyaei G, Jalaie S, Sajjadi E. The effect of Tai Chi exercises on postural stability and control in older patients with knee osteoarthritis. Journal of bodywork and movement therapies. 2017;21(3):594–8. 10.1016/j.jbmt.2016.09.001
    1. Lee KY, Hui-Chan CW, Tsang WW. The effects of practicing sitting Tai Chi on balance control and eye-hand coordination in the older adults: a randomized controlled trial. Disability and rehabilitation. 2015;37(9):790–4. 10.3109/09638288.2014.942003
    1. Wong AM, Chou S-W, Huang S-C, Lan C, Chen H-C, Hong W-H, et al. Does different exercise have the same effect of health promotion for the elderly? Comparison of training-specific effect of Tai Chi and swimming on motor control. Archives of gerontology and geriatrics. 2011;53(2):e133–e7. 10.1016/j.archger.2010.07.009
    1. Wei G, Xu T, Fan F, Dong H, Jiang L, Li H. Can Taichi reshape the brain. A brain morph. 2013. 10.1371/journal.pone.0061038

Source: PubMed

3
購読する