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Multimodal physical activity increases brain-derived neurotrophic factor levels and improves cognition in institutionalized older women

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Abstract

Physical activity has been proposed as a promising intervention to improve cognition and decrease the risk of dementia in older adults. Brain-derived neurotrophic factor (BDNF) appears to mediate, at least partially, these effects of exercise. However, intervention studies of the effects of multimodal exercises on cognition and BDNF levels are scarce and composed by small samples. Thus, the generalization of the conclusions of these studies depends on the reproducibility of the results. In order to contribute to the knowledge on the field, the present study evaluated the effects of a physical activity intervention composed by muscle strengthening and aerobic conditioning on BDNF levels and cognition in older women. Independent and non-demented subjects (≥75 years) were assigned to a 3-month physical activity intervention (n = 22, 60 min exercise sessions three times a week) or to a control condition (n = 10, no exercise). Clinical (anxiety and depression symptoms), neuropsychological (Digit Span, Stroop, Trail Making, and Contextual Memory tests), physical (upper and lower limb strength, aerobic conditioning), and physiological (serum BDNF) parameters were evaluated immediately before, 1 month, and 3 months after starting intervention. Results indicated that controls had stable levels for all measured variables, whereas the intervention group improved on physical fitness, depressive symptoms, cognitive performance, and BDNF levels. Moreover, a linear regression identified an association between aerobic conditioning and BDNF levels. In conclusion, combined muscle strengthening and aerobic conditioning was able to improve cognitive performance and increase BDNF levels. Aerobic conditioning seems to be an important mediator of these outcomes.

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References

  • Archer T, Josefsson T, Lindwall M (2014) Effects of physical exercise on depressive symptoms and biomarkers in depression. CNS Neurol Disord Drug Targets 13(10):1640–1653

    Article  PubMed  Google Scholar 

  • Baker LD, Frank LL, Foster-Schubert K, Green PS, Wilkinson CW, McTiernan A et al (2010a) Aerobic exercise improves cognition for older adults with glucose intolerance, a risk factor for Alzheimer’s disease. J Alzheimers Dis 22:569–579. doi:10.3233/jad-2010-100768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker LD, Frank LL, Foster-Schubert K, Green PS, Wilkinson CW, McTiernan A et al (2010b) Effects of aerobic exercise on mild cognitive impairment: a controlled trial. Arch Neurol 67:71–79. doi:10.1001/archneurol.2009.307

    PubMed  PubMed Central  Google Scholar 

  • Baltzopoulos V, Brodie DA (1989) Isokinetic dynamometry. Applications and limitations. Sports Med (Auckland, NZ) 8(2):101–116

    Article  CAS  Google Scholar 

  • Barulli D, Stern Y (2013) Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci 17(10):502–509. doi:10.1016/j.tics.2013.08.012

    Article  PubMed  Google Scholar 

  • Bean JF, Kiely DK, Leveille SG, Herman S, Huynh C, Fielding R, Frontera W (2002) The 6-minute walk test in mobility-limited elders: what is being measured? J Gerontol A Biol Sci Med Sci 57:M751–M756

    Article  PubMed  Google Scholar 

  • Beeri MS, Sonnen J (2016) Brain BDNF expression as a biomarker for cognitive reserve against Alzheimer disease progression. Neurology. United States. doi:10.1212/WNL.0000000000002389

  • Bekinschtein P, Cammarota M, Izquierdo I, Medina JH (2008) BDNF and memory formation and storage. Neurosci Rev J Bringing Neurobiol Neurol Psychiatr 14(2):147–156. doi:10.1177/1073858407305850

    CAS  Google Scholar 

  • Bertolucci PH, Brucki SM, Campacci SR, Juliano Y (1994) The Mini-Mental State Examination in a general population: impact of educational status. Arq Neuropsiquiatr 52(1):1–7

    Article  CAS  PubMed  Google Scholar 

  • Blair SN, Dowda M, Pate RR, Kronenfeld J, Howe HGJ, Parker G et al (1991) Reliability of long-term recall of participation in physical activity by middle-aged men and women. Am J Epidemiol 133(3):266–275

    Article  CAS  PubMed  Google Scholar 

  • Bus BAA, Molendijk ML, Penninx BJWH, Buitelaar JK, Kenis G, Prickaerts J et al (2011) Determinants of serum brain-derived neurotrophic factor. Psychoneuroendocrinology 36(2):228–239. doi:10.1016/j.psyneuen.2010.07.013

    Article  CAS  PubMed  Google Scholar 

  • Bus BAA, Tendolkar I, Franke B, de Graaf J, den Heijer M, Buitelaar JK, Oude Voshaar RC (2012) Serum brain-derived neurotrophic factor: determinants and relationship with depressive symptoms in a community population of middle-aged and elderly people. World J Biol Psychiatr Off J World Fed Soc Biol Psychiatr 13(1):39–47. doi:10.3109/15622975.2010.545187

    Article  Google Scholar 

  • Carlino D, De Vanna M, Tongiorgi E (2013) Is altered BDNF biosynthesis a general feature in patients with cognitive dysfunctions? Neurosci Rev J Bringing Neurobiol Neurol Psychiatr 19(4):345–353. doi:10.1177/1073858412469444

    CAS  Google Scholar 

  • Carvalho A, Rea IM, Parimon T, Cusack BJ (2014) Physical activity and cognitive function in individuals over 60 years of age: a systematic review. Clin Interv Aging 9:661–682. doi:10.2147/CIA.S55520

    PubMed  PubMed Central  Google Scholar 

  • Chan KL, Tong KY, Yip SP (2008) Relationship of serum brain-derived neurotrophic factor (BDNF) and health-related lifestyle in healthy human subjects. Neurosci Lett 447(2–3):124–128. doi:10.1016/j.neulet.2008.10.013

    Article  CAS  PubMed  Google Scholar 

  • Chodzko-Zajko WJ, Proctor DN, Fiatarone Singh MA, Minson CT, Nigg CR, Salem GJ, Skinner JS (2009) American College of Sports Medicine position stand. Exercise and physical activity for older adults. Med Sci Sports Exerc 41(7):1510–1530. doi:10.1249/MSS.0b013e3181a0c95c

    Article  PubMed  Google Scholar 

  • Coelho FG, Gobbi S, Andreatto CA, Corazza DI, Pedroso RV, Santos-Galduroz RF (2013) Physical exercise modulates peripheral levels of brain-derived neurotrophic factor (BDNF): a systematic review of experimental studies in the elderly. Arch Gerontol Geriatr 56:10–15. doi:10.1016/j.archger.2012.06.003

    Article  CAS  PubMed  Google Scholar 

  • Colcombe S, Kramer AF (2003) Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci 14:125–130

    Article  PubMed  Google Scholar 

  • Correa MS, Vedovelli K, Giacobbo BL, de Souza CEB, Ferrari P, de Lima Argimon II et al (2015) Psychophysiological correlates of cognitive deficits in family caregivers of patients with Alzheimer disease. Neuroscience 286:371–382. doi:10.1016/j.neuroscience.2014.11.052

    Article  CAS  PubMed  Google Scholar 

  • Cunha JA (2011) Escalas Beck—manual, 1st edn. Casa do Psicólogo, São Paulo

    Google Scholar 

  • Desjardins-Crepeau L, Berryman N, Fraser SA, Vu TTM, Kergoat M-J, Li KZ et al (2016) Effects of combined physical and cognitive training on fitness and neuropsychological outcomes in healthy older adults. Clin Interv Aging 11:1287–1299

    Article  PubMed  PubMed Central  Google Scholar 

  • Erickson KI, Prakash RS, Voss MW, Chaddock L, Heo S, McLaren M et al (2010) Brain-derived neurotrophic factor is associated with age-related decline in hippocampal volume. J Neurosci Off J Soc Neurosci 30(15):5368–5375. doi:10.1523/JNEUROSCI.6251-09.2010

    Article  CAS  Google Scholar 

  • Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L et al (2011) Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A 108(7):3017–3022. doi:10.1073/pnas.1015950108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erickson KI, Miller DL, Roecklein KA (2012) The aging hippocampus: interactions between exercise, depression, and BDNF. Neurosci Rev J Bringing Neurobiol Neurol Psychiatr 18(1):82–97. doi:10.1177/1073858410397054

    CAS  Google Scholar 

  • Fleg JL (2002) Can exercise conditioning be effective in older heart failure patients? Heart Fail Rev 7(1):99–103

    Article  PubMed  Google Scholar 

  • Floel A, Ruscheweyh R, Kruger K, Willemer C, Winter B, Volker K et al (2010) Physical activity and memory functions: are neurotrophins and cerebral gray matter volume the missing link? NeuroImage 49:2756–2763. doi:10.1016/j.neuroimage.2009.10.043

    Article  CAS  PubMed  Google Scholar 

  • Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  CAS  PubMed  Google Scholar 

  • Gunstad J, Benitez A, Smith J, Glickman E, Spitznagel MB, Alexander T et al (2008) Serum brain-derived neurotrophic factor is associated with cognitive function in healthy older adults. J Geriatr Psychiatry Neurol 21:166–170. doi:10.1177/0891988708316860

    Article  PubMed  Google Scholar 

  • Jaureguizar KV, Vicente-Campos D, Bautista LR, de la Pena CH, Gomez MJA, Rueda MJC, Fernandez Mahillo I (2016) Effect of high-intensity interval versus continuous exercise training on functional capacity and quality of life in patients with coronary artery disease: a randomized clinical trial. J Cardiopulm Rehabil Prev 36(2):96–105. doi:10.1097/HCR.0000000000000156

    Article  PubMed  Google Scholar 

  • Jones CJ, Rikli RE, Beam WC (1999) A 30-s chair-stand test as a measure of lower body strength in community-residing older adults. Res Q Exerc Sport 70:113–119

    Article  CAS  PubMed  Google Scholar 

  • Kern H, Hofer C, Modlin M, Forstner C, Raschka-Hogler D, Mayr W, Stohr H (2002) Denervated muscles in humans: limitations and problems of currently used functional electrical stimulation training protocols. Artif Organs 26(3):216–218

    Article  PubMed  Google Scholar 

  • Leal G, Bramham CRR, Duarte CBB (2017) BDNF and hippocampal synaptic plasticity. Vitam Horm 104:153–195. doi:10.1016/bs.vh.2016.10.004

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Kim J, Han ES, Chae S, Ryu M, Ahn KH, Park EJ (2015) Changes in physical activity and cognitive decline in older adults living in the community. Age (Dordr) 37(2):20. doi:10.1007/s11357-015-9759-z

    Article  Google Scholar 

  • Lista I, Sorrentino G (2010) Biological mechanisms of physical activity in preventing cognitive decline. Cell Mol Neurobiol 30:493–503. doi:10.1007/s10571-009-9488-x

    Article  CAS  PubMed  Google Scholar 

  • Lommatzsch M, Zingler D, Schuhbaeck K, Schloetcke K, Zingler C, Schuff-Werner P, Virchow JC (2005) The impact of age, weight and gender on BDNF levels in human platelets and plasma. Neurobiol Aging 26(1):115–123. doi:10.1016/j.neurobiolaging. 2004.03.002

    Article  CAS  PubMed  Google Scholar 

  • Lustosa LP, Silva JP, Coelho FM, Pereira DS, Parentoni AN, Pereira LSM (2011) Impact of resistance exercise program on functional capacity and muscular strength of knee extensor in pre-frail community-dwelling older women: a randomized crossover trial. Revista Brasileira de Fisioterapia (Sao Carlos (Sao Paulo, Brazil)) 15(4):318–324

    Article  Google Scholar 

  • Martinowich K, Manji H, Lu B (2007) New insights into BDNF function in depression and anxiety. Nat Neurosci 10:1089–1093. doi:10.1038/nn1971

    Article  CAS  PubMed  Google Scholar 

  • Nascimento CMC, Pereira JR, de Andrade LP, Garuffi M, Talib LL, Forlenza OV et al (2014) Physical exercise in MCI elderly promotes reduction of pro-inflammatory cytokines and improvements on cognition and BDNF peripheral levels. Curr Alzheimer Res 11(8):799–805

    Article  PubMed  Google Scholar 

  • Neeper SA, Gomez-Pinilla F, Choi J, Cotman C (1995) Exercise and brain neurotrophins. Nature. England. doi:10.1038/373109a0

  • Novkovic T, Mittmann T, Manahan-Vaughan D (2015) BDNF contributes to the facilitation of hippocampal synaptic plasticity and learning enabled by environmental enrichment. Hippocampus 25(1):1–15. doi:10.1002/hipo.22342

    Article  CAS  PubMed  Google Scholar 

  • O’Bryant SE, Hobson VL, Hall JR, Barber RC, Zhang S, Johnson L et al, Texas Alzheimer’s Res C (2011) Serum brain-derived neurotrophic factor levels are specifically associated with memory performance among Alzheimer’s disease cases. Dement Geriatr Cogn Disord 31:31–36. doi:10.1159/000321980

  • Pahor M, Guralnik JM, Ambrosius WT, Blair S, Bonds DE, Church TS et al (2014) Effect of structured physical activity on prevention of major mobility disability in older adults: the LIFE study randomized clinical trial. JAMA 311(23):2387–2396. doi:10.1001/jama.2014.5616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park H, Poo M (2013) Neurotrophin regulation of neural circuit development and function. Nat Rev Neurosci 14(1):7–23. doi:10.1038/nrn3379

    Article  CAS  PubMed  Google Scholar 

  • Pereira DS, de Queiroz BZ, Miranda AS, Rocha NP, Felicio DC, Mateo EC et al (2013) Effects of physical exercise on plasma levels of brain-derived neurotrophic factor and depressive symptoms in elderly women—a randomized clinical trial. Arch Phys Med Rehabil 94:1443–1450. doi:10.1016/j.apmr.2013.03.029

    Article  PubMed  Google Scholar 

  • Prince M, Bryce R, Albanese E, Wimo A, Ribeiro W, Ferri CP (2013) The global prevalence of dementia: a systematic review and metaanalysis. Alzheimer’s Dement J Alzheimer’s Assoc 9(1):63–75.e2. doi:10.1016/j.jalz.2012.11.007

    Article  Google Scholar 

  • Rasmussen P, Brassard P, Adser H, Pedersen MV, Leick L, Hart E et al (2009) Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp Physiol 94:1062–1069. doi:10.1113/expphysiol.2009.048512

    Article  CAS  PubMed  Google Scholar 

  • Rosas-Vargas H, Martinez-Ezquerro JD, Bienvenu T (2011) Brain-derived neurotrophic factor, food intake regulation, and obesity. Arch Med Res 42(6):482–494. doi:10.1016/j.arcmed.2011.09.005

    Article  CAS  PubMed  Google Scholar 

  • Solway S, Brooks D, Lacasse Y, Thomas S (2001) A qualitative systematic overview of the measurement properties of functional walk tests used in the cardiorespiratory domain. Chest 119:256–270

    Article  CAS  PubMed  Google Scholar 

  • Strait JBJ, Lakatta EEG (2012) Aging-associated cardiovascular changes and their relationship to heart failure. Heart Fail Clin 8(1):143–164. doi:10.1016/j.hfc.2011.08.011.Aging-associated

    Article  PubMed  PubMed Central  Google Scholar 

  • Strath SJ, Swartz AM, Bassett DRJ, O’Brien WL, King GA, Ainsworth BE (2000) Evaluation of heart rate as a method for assessing moderate intensity physical activity. Med Sci Sports Exerc 32(9 Suppl):S465–S470

    Article  CAS  PubMed  Google Scholar 

  • Strauss E, Spreen O, Sherman EMS (2006) A Compendium of Neuropsychological Tests: Administration, Norms, And Commentary. 3rd ed. Oxford University Press, editor, New York, p 1216

  • Suzuki T, Shimada H, Makizako H, Doi T, Yoshida D, Ito K et al (2013) A randomized controlled trial of multicomponent exercise in older adults with mild cognitive impairment. PLoS One 8(4):e61483. doi:10.1371/journal.pone.0061483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tadjibaev P, Frolova E, Gurina N, Degryse J, Vaes B (2014) The relationship between physical performance and cardiac function in an elderly Russian cohort. Arch Gerontol Geriatr 59(3):554–561. doi:10.1016/j.archger.2014.08.003

    Article  PubMed  Google Scholar 

  • Tarazona-Santabalbina FJ, Gomez-Cabrera MC, Perez-Ros P, Martinez-Arnau FM, Cabo H, Tsaparas K et al (2016) A multicomponent exercise intervention that reverses frailty and improves cognition, emotion, and social networking in the community-dwelling frail elderly: a randomized clinical trial. J Am Med Dir Assoc 17(5):426–433. doi:10.1016/j.jamda.2016.01.019

    Article  PubMed  Google Scholar 

  • Vaes B, Rezzoug N, Pasquet A, Wallemacq P, Van Pottelbergh G, Mathei C et al (2012) The prevalence of cardiac dysfunction and the correlation with poor functioning among the very elderly. Int J Cardiol 155(1):134–143. doi:10.1016/j.ijcard.2011.07.024

    Article  PubMed  Google Scholar 

  • Van der Bij AK, Laurant MGH, Wensing M (2002) Effectiveness of physical activity interventions for older adults: a review. Am J Prev Med 22(2):120–133

    Article  PubMed  Google Scholar 

  • Vaughan S, Wallis M, Polit D, Steele M, Shum D, Morris N (2014) The effects of multimodal exercise on cognitive and physical functioning and brain-derived neurotrophic factor in older women: a randomised controlled trial. Age Ageing 43(5):623–629. doi:10.1093/ageing/afu010

    Article  PubMed  Google Scholar 

  • Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20:2580–2590. doi:10.1111/j.1460-9568.2004.03720.x

    Article  PubMed  Google Scholar 

  • Volpi E, Nazemi R, Fujita S (2004) Muscle tissue changes with aging. Curr Opin Clin Nutr Metab Care 7(4):405–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ward DD, Summers MJ, Saunders NL, Ritchie K, Summers JJ, Vickers JC (2015) The BDNF Val66Met polymorphism moderates the relationship between cognitive reserve and executive function. Transl Psychiatry 5:e590. doi:10.1038/tp.2015.82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe Y, Madarame H, Ogasawara R, Nakazato K, Ishii N (2014) Effect of very low-intensity resistance training with slow movement on muscle size and strength in healthy older adults. Clin Physiol Funct Imaging 34(6):463–470. doi:10.1111/cpf.12117

    Article  PubMed  Google Scholar 

  • Wechsler D (1987) Manual for the Wechsler Memory Scale—revised. The psychological Corporation

  • Wechsler D (1997) WAIS III: Administration and Scoring Manual. Harcourt, editor. San Antonio, TX

  • Wei Z, Liao J, Qi F, Meng Z, Pan S (2015) Evidence for the contribution of BDNF-TrkB signal strength in neurogenesis: an organotypic study. Neurosci Lett 606:48–52. doi:10.1016/j.neulet.2015.08.032

    Article  CAS  PubMed  Google Scholar 

  • Wolfson L, Judge J, Whipple R, King M (1995) Strength is a major factor in balance, gait, and the occurrence of falls. J Gerontol A Biol Sci Med Sci 50 Spec No:64–67

    PubMed  Google Scholar 

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Acknowledgments

E. Bromberg and I.I.L. Argimon are National Counsel of Technological and Scientific Development (CNPq) research fellows. K. Vedovelli has a Research Support Foundation of Rio Grande do Sul (FAPERGS)/Coordination for the Improvement of Higher Education Personnel (CAPES) fellowship, and B.L. Giacobbo, M.S. Corrêa, and A. Wieck have a CAPES fellowship.

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Authors and Affiliations

  1. Laboratory of Biology and Development of the Nervous System, Faculty of Biosciences, Pontifical Catholic University of Rio Grande do Sul, Ipiranga Av., 6681, Building 12D, room 34, Porto Alegre, RS, 90619-900, Brazil

    Kelem Vedovelli, Bruno Lima Giacobbo, Márcio Silveira Corrêa & Elke Bromberg

  2. Graduate Program in Biomedical Gerontology, Pontifical Catholic University of Rio Grande do Sul, Ipiranga Av., 6690, Third Floor, Porto Alegre, RS, 90610-000, Brazil

    Kelem Vedovelli, Andréa Wieck, Irani Iracema de Lima Argimon & Elke Bromberg

  3. National Institute for Translational Medicine (INCT-TM), Porto Alegre, RS, Brazil

    Kelem Vedovelli, Bruno Lima Giacobbo, Márcio Silveira Corrêa & Elke Bromberg

  4. Graduate Program in Cellular and Molecular Biology, Pontifical Catholic University of Rio Grande do Sul, Ipiranga Av., 6681, building 12A, Second Floor, Porto Alegre, RS, 90619-900, Brazil

    Bruno Lima Giacobbo, Márcio Silveira Corrêa & Elke Bromberg

  5. Laboratory of Immunosenescence, Institute of Biomedical Research, Pontifical Catholic University of Rio Grande do Sul, Porto Alegre, Brazil

    Andréa Wieck

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  1. Kelem Vedovelli
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Correspondence to Elke Bromberg.

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The study was conducted in accordance with the ethical standards of the 1964 Declaration of Helsinki and approved by the Research and Ethics Committee of Pontifical Catholic University, Porto Alegre, Brazil. All participants gave their written informed consent.

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Vedovelli, K., Giacobbo, B.L., Corrêa, M.S. et al. Multimodal physical activity increases brain-derived neurotrophic factor levels and improves cognition in institutionalized older women. GeroScience 39, 407–417 (2017). https://doi.org/10.1007/s11357-017-9987-5

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