Physical activity to improve cognition in older adults: can physical activity programs enriched with cognitive challenges enhance the effects? A systematic review and meta-analysis

Freja Gheysen, Louise Poppe, Ann DeSmet, Stephan Swinnen, Greet Cardon, Ilse De Bourdeaudhuij, Sebastien Chastin, Wim Fias, Freja Gheysen, Louise Poppe, Ann DeSmet, Stephan Swinnen, Greet Cardon, Ilse De Bourdeaudhuij, Sebastien Chastin, Wim Fias

Abstract

Background: Aging-related cognitive decline and cognitive impairment greatly impacts older adults' daily life. The worldwide ageing of the population and associated wave of dementia urgently calls for prevention strategies to reduce the risk of cognitive decline. Physical activity (PA) is known to improve cognitive function at older age through processes of neuroplasticity. Yet, emerging studies suggest that larger cognitive gains may be induced when PA interventions are combined with cognitive activity (CA). This meta-analysis evaluates these potential synergistic effects by comparing cognitive effects following combined PA + CA interventions to PA interventions (PA only), CA interventions (CA only) and control groups.

Methods: Pubmed, Embase, PsycInfo, CINAHL and Sportdiscus were searched for English peer-reviewed papers until April 2018. Data were extracted on cognition and factors potentially influencing the cognitive effects: mode of PA + CA combination (sequential or simultaneous), session frequency and duration, intervention length and study quality. Differences between older adults with and without mild cognitive impairments were also explored.

Results: Forty-one studies were included. Relative to the control group, combined PA + CA intervention showed significantly larger gains in cognition (g = 0.316; 95% CI 0.188-0.443; p < .001). Studies that compared combined PA + CA with PA only, showed small but significantly greater cognitive improvement in favor of combined interventions (g = 0.160; 95% CI 0.041-0.279; p = .008). No significant difference was found between combined PA + CA and CA only interventions. Furthermore, cognitive effects tended to be more pronounced for studies using simultaneous designs (g = 0.385; 95%CI 0.214-0.555; p < .001) versus sequential designs (g = 0.114; 95%CI -0.102- 0.331, p = .301). Effects were not moderated by session frequency, session duration, intervention length or study quality. Also, no differences in effects were found between older adults with and without mild cognitive impairments.

Conclusion: Findings of the current meta-analysis suggest that PA programs for older adults could integrate challenging cognitive exercises to improve cognitive health. Combined PA + CA programs should be promoted as a modality for preventing as well as treating cognitive decline in older adults. Sufficient cognitive challenge seems more important to obtain cognitive effects than high doses of intervention sessions.

Keywords: Cognition; Cognitive activity; Cognitive impairment; Combined intervention; Meta-analysis; Older adults; Physical activity.

Conflict of interest statement

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Flow chart of study selection process
Fig. 2
Fig. 2
Forest plot of effect sizes for combined PA + CA versus control
Fig. 3
Fig. 3
Forest plot of effect sizes for combined PA + CA versus PA only
Fig. 4
Fig. 4
Forest plot of effect sizes for combined PA + CA versus CA only

References

    1. World Health Organization . Governments commit to advancements in dementia research and care. Geneva, Switzerland. 2015.
    1. Gutchess A. Plasticity of the aging brain: new directions in cognitive neuroscience. Science. 2014;346(6209):579–582. doi: 10.1126/science.1254604.
    1. Reuter-Lorenz PA, Park DC. Human neuroscience and the aging mind: at old problems a new look. J Gerontol B Psychol Sci Soc Sci. 2010;65(4):405–415. doi: 10.1093/geronb/gbq035.
    1. Northey JM, Cherbuin N, Pumpa KL, Smee DJ, Rattray B. Exercise interventions for cognitive function in adults older than 50: a systematic review with meta-analysis. Br J Sports Med. 2017;0:1–9.
    1. Norton S, Matthews FE, Barnes DE, Yaffe K, Brayne C. Potential for primary prevention of Alzheimer’s disease: an analysis of population-based data. Lancet Neurol. 2014;13(8):788–794. doi: 10.1016/S1474-4422(14)70136-X.
    1. Panza GA, Taylor BA, MacDonald HV, Johnson BT, Zaleski AL, Livingston J, et al. J am Geriatr Soc. 2018. Can exercise improve cognitive symptoms of Alzheimer's disease? A meta-analysis.
    1. Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, et al. Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci. 2006;61(11):1166–1170. doi: 10.1093/gerona/61.11.1166.
    1. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. Exercise training increases size of hippocampus and improves memory. PNAS. 2011;(7):3017–22.
    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;5:26. doi: 10.3389/fnhum.2011.00026.
    1. Voss MW, Prakash RS, Erickson KI. Plasticity of brain networks in a randomized intervention trial of exercise training in older adults. Front Aging Neurosci. 2010;2:1–17.
    1. Fissler P, Küster O, Schlee W, Kolassa I-T. Novelty interventions to enhance broad cognitive abilities and prevent dementia: synergistic approaches for the facilitation of positive plastic change. Prog Brain Res. 2013;207:403–434. doi: 10.1016/B978-0-444-63327-9.00017-5.
    1. Langdon KD, Corbett D. Improved working memory following novel combinations of physical and cognitive activity. Neurorehabil Neural Repair. 2012;26(5):523–532. doi: 10.1177/1545968311425919.
    1. Smith AM, Spiegler KM, Sauce B, Wass CD, Sturzoiu T, Matzel LD. Voluntary aerobic exercise increases the cognitive enhancing effects of working memory training. Behav Brain Res. 2013;256:626–635. doi: 10.1016/j.bbr.2013.09.012.
    1. Law LLF, Barnett F, Yau MK, Gray MA. Effects of combined cognitive and exercise interventions on cognition in older adults with and without cognitive impairment: a systematic review. Ageing Res Rev. 2014;15:61–75. doi: 10.1016/j.arr.2014.02.008.
    1. Lauenroth A, Ioannidis AE, Teichmann B. Influence of combined physical and cognitive training on cognition: a systematic review. BMC Geriatr. 2016;16:141. doi: 10.1186/s12877-016-0315-1.
    1. Zhu X, Yin S, Lang M, He R, Li J. The more the better? A meta-analysis on effects of combined cognitive and physical intervention on cognition in healthy older adults. Ageing Res Rev. 2016;31:67–79. doi: 10.1016/j.arr.2016.07.003.
    1. Stanmore E, Stubbs B, Vancampfort D, de Bruin ED, Firth J. The effect of active video games on cognitive functioning in clinical and non-clinical populations: a meta-analysis of randomized controlled trials. Neurosci Biobehav Rev. 2017;78:34–43. doi: 10.1016/j.neubiorev.2017.04.011.
    1. Dhami P, Moreno S, DeSouza JFX. New framework for rehabilitation - fusion of cognitive and physical rehabilitation: the hope for dancing. Front Psychol. 2014;5:1478.
    1. Kattenstroth J-C, Kalisch T, Holt S, Tegenthoff M, Dinse HR. Six months of dance intervention enhances postural, sensorimotor, and cognitive performance in elderly without affecting cardio-respiratory functions. Front Aging Neurosci. 2013;5:5. doi: 10.3389/fnagi.2013.00005.
    1. Ainsworth BE, Haskell WL, Herrmann SD, Meckes N, Bassett DR, Jr, Tudor-Locke C, et al. 2011 compendium of physical activities: a second update of codes and MET values. Med Sci Sports Exerc. 2011;43(8):1575–1581. doi: 10.1249/MSS.0b013e31821ece12.
    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):261–279. doi: 10.1123/japa.18.3.261.
    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. J Am Geriatr Soc. 2014;62(1):25–39. doi: 10.1111/jgs.12611.
    1. Knaepen K, Goekint M, Heyman EM, Meeusen R. Neuroplasticity – exercise-induced response of peripheral brain-derived neurotrophic factor. Sports Med. 2010;40(9):765–801. doi: 10.2165/11534530-000000000-00000.
    1. Hedges L. Distribution theory for Glass’s estimator of effect size and related estimators. J Educ Stat. 1981;6:128. doi: 10.3102/10769986006002107.
    1. Ansai JH, de Andrade LP, de Souza Buto MS, de Vassimon Barroso Carmelo V, Farche AC, Rossi PG, et al. Effects of the addition of a dual task to a supervised physical exercise program on older adults’ cognitive performance. J Aging Phys Act. 2016;25:234–239. doi: 10.1123/japa.2016-0094.
    1. Barnes DE, Santos-Modesitt W, Poelke G, Kramer AF, Castro C, Middleton LE, et al. The mental activity and exercise (MAX) trial: a randomized controlled trial to enhance cognitive function in older adults. JAMA Intern Med. 2013;173(9):797–804. doi: 10.1001/jamainternmed.2013.189.
    1. Desjardins-Crepeau L, Berryman N, Fraser SA, Vu TT, Kergoat MJ, Li KZ, et al. Effects of combined physical and cognitive training on fitness and neuropsychological outcomes in healthy older adults. Clin Interv Aging. 2016;11:1287–1299. doi: 10.2147/CIA.S115711.
    1. Eggenberger P, Schumacher V, Angst M, Theill N, de Bruin ED, Author A, et al. Does multicomponent physical exercise with simultaneous cognitive training boost cognitive performance in older adults? A 6-month randomized controlled trial with a 1-year follow-up. Clin Interv Aging. 2015;10:1335–1349.
    1. Eggenberger P, Wolf M, Schumann M, de Bruin ED. Exergame and balance training modulate prefrontal brain activity during walking and enhance executive function in older adults. Front Aging Neurosci. 2016;8:66. doi: 10.3389/fnagi.2016.00066.
    1. Fabre C, Chamari K, Mucci P, Masse-Biron J, Prefaut C. Improvement of cognitive function by mental and/or individualized aerobic training in healthy elderly subjects. Int J Sports Med. 2002;23(6):415–421. doi: 10.1055/s-2002-33735.
    1. Fiatarone Singh MA, Gates N, Saigal N, Wilson GC, Meiklejohn J, Brodaty H, et al. The study of mental and resistance training (SMART) study-resistance training and/or cognitive training in mild cognitive impairment: a randomized, double-blind, double-sham controlled trial. J Am Med Dir Assoc. 2014;15(12):873–880. doi: 10.1016/j.jamda.2014.09.010.
    1. Hackney ME, Byers C, Butler G, Sweeney M, Rossbach L, Bozzorg A, et al. Adapted tango improves mobility, motor-cognitive function, and gait but not cognition in older adults in independent living. J Am Geriatr Soc. 2015;63(10):2105–2113. doi: 10.1111/jgs.13650.
    1. Hagovska M, Nagyova I. The transfer of skills from cognitive and physical training to activities of daily living: a randomised controlled study. Eur J Ageing. 2016;14:133–142. doi: 10.1007/s10433-016-0395-y.
    1. Hiyamizu M, Morioka S, Shomoto K, Shimada T. Effects of dual task balance training on dual task performance in elderly people: a randomized controlled trial. Clin Rehabil. 2012;26(1):58–67. doi: 10.1177/0269215510394222.
    1. Hughes TF, Flatt JD, Fu B, Butters MA, Chang CCH, Ganguli M, et al. Interactive video gaming compared with health education in older adults with mild cognitive impairment: a feasibility study. Int J Geriatr Psychiatry. 2014;29(9):890–898. doi: 10.1002/gps.4075.
    1. Jansen P, Dahmen-Zimmer K. Effects of cognitive, motor, and karate training on cognitive functioning and emotional well-being of elderly people. Front Psychol. 2012;3:40. doi: 10.3389/fpsyg.2012.00040.
    1. Kim SH, Kim M, Ahn YB, Lim HK, Kang SG, Cho JH, et al. Effect of dance exercise on cognitive function in elderly patients with metabolic syndrome: a pilot study. J Sports Sci Med. 2011;10(4):671–678.
    1. Kitazawa K, Showa S, Hiraoka A, Fushiki Y, Sakauchi H, Mori M. Effect of a dual-task net-step exercise on cognitive and gait function in older adults. J Geriatr Phys Ther. 2015;38(3):133–140. doi: 10.1519/JPT.0000000000000029.
    1. Lam LCW, Chau RCM, Wong BML, Fung AWT, Tam CWC, Leung GTY, 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.e15-.e20. doi: 10.1016/j.jamda.2012.03.008.
    1. Legault C, Jennings JM, Katula JA, Dagenbach D, Gaussoin SA, Sink KM, et al. Designing clinical trials for assessing the effects of cognitive training and physical activity interventions on cognitive outcomes: the seniors health and activity research program pilot (SHARP-P) study, a randomized controlled trial. BMC Geriatr. 2011;11:27. doi: 10.1186/1471-2318-11-27.
    1. León J, Ureña A, Bolaños MJ, Bilbao A, Oña A. A combination of physical and cognitive exercise improves reaction time in persons 61-84 years old. J Aging Phys Activ. 2015;23(1):72–77. doi: 10.1123/JAPA.2012-0313.
    1. Li F, Harmer P, Liu Y, Chou LS, et al. Tai Ji Quan and global cognitive function in older adults with cognitive impairment: a pilot study. Arch Gerontol Geriatr. 2014;58(3):434–439. doi: 10.1016/j.archger.2013.12.003.
    1. Lu X, Siu KC, Fu SN, Hui-Chan CWY, Tsang WWN. Effects of tai chi training on postural control and cognitive performance while dual tasking - a randomized clinical trial. J Complement Integr Med. 2016;13(2):181–187. doi: 10.1515/jcim-2015-0084.
    1. Maillot P, Perrot A, Hartley A, et al. Effects of interactive physical-activity video-game training on physical and cognitive function in older adults. Psychol Aging. 2012;27(3):589–600. doi: 10.1037/a0026268.
    1. Merom D, Grunseit A, Eramudugolla R, Jefferis B, Mcneill J, Anstey KJ. Cognitive benefits of social dancing and walking in old age: the dancing mind randomized controlled trial. Front Aging Neurosci. 2016;8:26. doi: 10.3389/fnagi.2016.00026.
    1. Nishiguchi S, Yamada M, Tanigawa T, Sekiyama K, Kawagoe T, Suzuki M, et al. A 12-week physical and cognitive exercise program can improve cognitive function and neural efficiency in community-dwelling older adults: a randomized controlled trial. J Am Geriatr Soc. 2015;63(7):1355–1363. doi: 10.1111/jgs.13481.
    1. Oswald WD, Gunzelmann T, Rupprecht R, Hagen B. Differential effects of single versus combined cognitive and physical training with older adults: the SimA study in a 5-year perspective. Eur J Ageing. 2006;3(4):179–192. doi: 10.1007/s10433-006-0035-z.
    1. Sato D, Seko C, Hashitomi T, Sengoku Y, Nomura T. Differential effects of water-based exercise on the cognitive function in independent elderly adults. Aging Clin Exp Res. 2015;27(2):149–159. doi: 10.1007/s40520-014-0252-9.
    1. Schättin A, Arner R, Gennaro F, de Bruin ED. Adaptations of prefrontal brain activity, executive functions, and gait in healthy elderly following Exergame and balance training: a randomized-controlled study. Front Aging Neurosci. 2016;8:278.
    1. Shah T, Verdile G, Sohrabi H, Campbell A, Putland E, Cheetham C, et al. A combination of physical activity and computerized brain training improves verbal memory and increases cerebral glucose metabolism in the elderly. Transl Psychiatry. 2014;4:e487. doi: 10.1038/tp.2014.122.
    1. Styliadis C, Kartsidis P, Paraskevopoulos E, Ioannides AA, Bamidis PD, et al. Neuroplastic effects of combined computerized physical and cognitive training in elderly individuals at risk for dementia: an eLORETA controlled study on resting states. Neural Plast. 2015;2015:172192. doi: 10.1155/2015/172192.
    1. Suzuki T, Shimada H, Makizako H, Doi T, Yoshida D, Ito K, et al. A randomized controlled trial of multicomponent exercise in older adults with mild cognitive impairment. PLoS One. 2013;8:e61483. doi: 10.1371/journal.pone.0061483.
    1. Teixeira CVL, Gobbi S, Pereira JR, Vital TM, Hernandéz SSS, Shigematsu R, et al. Effects of square-stepping exercise on cognitive functions of older people. Psychogeriatrics. 2013;13(3):148–156. doi: 10.1111/psyg.12017.
    1. Theill N, Schumacher V, Adelsberger R, Martin M, Jäncke L, Author A, et al. Effects of simultaneously performed cognitive and physical training in older adults. BMC Neurosci. 2013;14:103. doi: 10.1186/1471-2202-14-103.
    1. van het Reve E, de Bruin ED. Strength-balance supplemented with computerized cognitive training to improve dual task gait and divided attention in older adults: a multicenter randomized-controlled trial. BMC Geriatr. 2014;14:134. doi: 10.1186/1471-2318-14-134.
    1. Witte K, Kropf S, Darius S, Emmermacher P, Böckelmann I, Author A, et al. Comparing the effectiveness of karate and fitness training on cognitive functioning in older adults-a randomized controlled trial. J Sport Health Sci. 2016;5:484–490. doi: 10.1016/j.jshs.2015.09.006.
    1. Yokoyama H, Okazaki K, Imai D, Yamashina Y, Takeda R, Naghavi N, et al. The effect of cognitive-motor dual-task training on cognitive function and plasma amyloid beta peptide 42/40 ratio in healthy elderly persons: a randomized controlled trial. BMC Geriatr. 2015;15:60. doi: 10.1186/s12877-015-0058-4.
    1. Damirchi A, Hosseini F, Babaei P. Mental training enhances cognitive function and BDNF more than either physical or combined training in elderly women with MCI: a small-scale study. Am J Alzheimers Dis Other Demen. 2018;33(1):20–29. doi: 10.1177/1533317517727068.
    1. Falbo S, Condello G, Capranica L, Forte R, Pesce C. Effects of physical-cognitive dual task training on executive function and gait performance in older adults: a randomized controlled trial. Biomed Res Int. 2016;2016:5812092. doi: 10.1155/2016/5812092.
    1. Müller P, Rehfeld K, Schmicker M, Hökelmann A, Dordevic M, Lessmann V, et al. Evolution of neuroplasticity in response to physical activity in old age: the case for dancing. Front Aging Neurosci. 2017;9:56.
    1. Schoene D, Lord SR, Delbaere K, Severino C, Davies TA, Smith ST. A randomized controlled pilot study of home-based step training in older people using videogame technology. PLoS One. 2013;8(3):e57734. doi: 10.1371/journal.pone.0057734.
    1. Siu M-Y, Lee DTF. Effects of tai chi on cognition and instrumental activities of daily living in community dwelling older people with mild cognitive impairment. BMC Geriatr. 2018;18(1):37. doi: 10.1186/s12877-018-0720-8.
    1. Sungkarat S, Boripuntakul S, Chattipakorn N, Watcharasaksilp K, Lord SR. Effects of tai chi on cognition and fall risk in older adults with mild cognitive impairment: a randomized controlled trial. J Am Geriatr Soc. 2017;65(4):721–727. doi: 10.1111/jgs.14594.
    1. Petersen RC. Mild cognitive impairment as a diagnostic entity. J Intern Med. 2004;256:183–194. doi: 10.1111/j.1365-2796.2004.01388.x.
    1. Saykin AJ, Wishart HA, Rabin LA, Santulli RB, Flashman LA, West JD, et al. Older adults with cognitive complaints show brain atrophy similar to that of amnestic MCI. Neurology. 2006;67:834–842. doi: 10.1212/01.wnl.0000234032.77541.a2.
    1. Wang Y, Risacher SL, West JD, McDonald BC, MaGee TR, Farlow MR, et al. Altered default mode network connectivity in older adults with cognitive complaints and amnestic mild cognitive impairment. J Alzheimers Dis. 2013;35:751–760. doi: 10.3233/JAD-130080.
    1. Hannan AJ. Environmental enrichment and brain repair: harnessing the therapeutic effects of cognitive stimulation and physical activity to enhance experience-dependent plasticity. Neuropathol Appl Neurobiol. 2014;40(1):13–25. doi: 10.1111/nan.12102.
    1. van Praag H, Shubert T, Zhao C, Gage FH. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci. 2005;25(38):8680–8685. doi: 10.1523/JNEUROSCI.1731-05.2005.
    1. Mustroph ML, Chen S, Desai SC, Cay EB, DeYoung EK, Rhodes JS. Aerobic exercise is the critical variable in an enriched environment that increases hippocampal neurogenesis and water maze learning in male C57BL/6J mice. Neuroscience. 2012;219:62–71. doi: 10.1016/j.neuroscience.2012.06.007.
    1. Fabel K. Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Front Neurosci. 2009;3:50.
    1. Shors TJ, Anderson ML, Curlik DM, Nokia MS. Use it or lose it: how neurogenesis keeps the brain fit for learning. Behav Brain Res. 2012;227(2):450–458. doi: 10.1016/j.bbr.2011.04.023.
    1. Boisgontier MP, Beets IAM, Duysens J, Nieuwboer A, Krampe RT, Swinnen SP. Age-related differences in attentional cost associated with postural dual tasks: increased recruitment of generic cognitive resources in older adults. Neurosci Biobehav Rev. 2013;37(8):1824–1837. doi: 10.1016/j.neubiorev.2013.07.014.
    1. Cotman C, Berchtold NC. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 2002;25(6):295–301. doi: 10.1016/S0166-2236(02)02143-4.
    1. Colcombe S, Kramer AF. Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci. 2003;14(2):125–130. doi: 10.1111/1467-9280.t01-1-01430.
    1. Nithianantharajah J, Hannan AJ. The neurobiology of brain and cognitive reserve: mental and physical activity as modulators of brain disorders. Prog Neurobiol. 2009;89(4):369–382. doi: 10.1016/j.pneurobio.2009.10.001.
    1. Zheng G, Xia R, Zhou W, Tao J, Chen L. Aerobic exercise ameliorates cognitive function in older adults with mild cognitive impairment: a systematic review and meta-analysis of randomised controlled trials. Br J Sports Med. 2016;50:1443–1450. doi: 10.1136/bjsports-2015-095699.

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere