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Effects of Physical Exercise on Plasma Levels of Brain-Derived Neurotrophic Factor and Depressive Symptoms in Elderly Women—A Randomized Clinical Trial

Published:April 22, 2013DOI:https://doi.org/10.1016/j.apmr.2013.03.029

      Abstract

      Objectives

      To investigate the effect of 2 standardized exercise programs, muscle strength exercises (SE) and aerobic exercises (AE), on the plasma levels of brain-derived neurotrophic factor (BDNF) and depressive symptoms in 451 elderly women.

      Design

      A randomized controlled trial.

      Setting

      Belo Horizonte/MG–Brazil.

      Participants

      Community-dwelling older women (N=451; age, 65–89y).

      Intervention

      The participants were divided into 2 groups: SE and AE. Both protocols lasted 10 weeks, and 30 sessions (1-h sessions) in total were performed 3 times a week under the direct supervision of physical therapists.

      Main Outcome Measures

      Plasma levels of BDNF (enzyme-linked immunosorbent assay) and depressive symptoms (Geriatric Depression Scale).

      Results

      There was a significant difference for BDNF plasma levels between the SE and AE groups (P=.009). Post hoc analysis revealed a pre-post intervention difference in BDNF levels only for the SE group (P=.008). A statistically significant difference was found for the pre- and postintervention Geriatric Depression Scale scores in both groups (P=.001), showing that the effects of both exercise protocols were comparable regarding depressive symptoms (P=.185).

      Conclusions

      The present findings have demonstrated the positive effect of muscle strengthening and aerobic intervention on depressive symptoms in community-dwelling elderly women. Interestingly, only SE significantly increased the plasma levels of BDNF in our sample. The positive effects of physical exercise on depressive symptoms in the elderly were not mediated by BDNF.

      Keywords

      List of abbreviations:

      AE (aerobic exercises), BDNF (brain-derived neurotrophic factor), GDS (Geriatric Depression Scale), RM (Repetition Maximum), SE (muscle exercises)
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      References

        • Murer M.G.
        • Yan Q.
        • Raisman-Vozari R.
        Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease.
        Prog Neurobiol. 2001; 63: 71-124
        • Hu Y.
        • Russek S.J.
        BDNF and the diseased nervous system: a delicate balance between adaptive and pathological processes of gene regulation.
        J Neurochem. 2008; 105: 1-17
        • Krabbe K.S.
        • Nielsen A.R.
        • Krogh-Madsen R.
        • et al.
        Brain-derived neurotrophic factor (BDNF) and type 2 diabetes.
        Diabetologia. 2007; 50: 431-438
        • Brunoni A.R.
        • Lopes M.
        • Fregni F.
        A systematic review and meta-analysis of clinical studies on major depression and BDNF levels: implications for the role of neuroplasticity in depression.
        Int J Neuropsychopharmacol. 2008; 11: 1169-1180
        • Sen S.
        • Duman R.
        • Sanacora G.
        Serum brain-derived neurotrophic factor, depression, and antidepressant medications: meta-analyses and implications.
        Biol Psychiatry. 2008; 64: 527-532
        • Karege F.
        • Perret G.
        • Bondolfi G.
        • Schwald M.
        • Bertschy G.
        • Aubry J.M.
        Decreased serum brain-derived neurotrophic factor levels in major depressed patients.
        Psychiatry Res. 2002; 109: 143-148
        • Scalzo P.
        • Kummer A.
        • Bretas T.L.
        • Cardoso F.
        • Teixeira A.L.
        Serum levels of brain-derived neurotrophic factor correlate with motor impairment in Parkinson's disease.
        J Neurol. 2010; 257: 540-545
        • Yasutake C.
        • Kuroda K.
        • Yanagawa T.
        • Okamura T.
        • Yoneda H.
        Serum BDNF, TNF-alpha and IL-1beta levels in dementia patients: comparison between Alzheimer's disease and vascular dementia.
        Eur Arch Psychiatry Clin Neurosci. 2006; 256: 402-406
        • Diniz B.S.
        • Teixeira A.L.
        Brain-derived neurotrophic factor and Alzheimer's disease: physiopathology and beyond.
        Neuromolecular Med. 2011; 13: 217-222
        • Forlenza O.V.
        • Diniz B.S.
        • Gattaz W.F.
        Diagnosis and biomarkers of predementia in Alzheimer's disease.
        BMC Med. 2010; 8: 89
        • Laske C.
        • Banschbach S.
        • Stransky E.
        • et al.
        Exercise-induced normalization of decreased BDNF serum concentration in elderly women with remitted major depression.
        Int J Neuropsychopharmacol. 2010; 13: 595-602
        • Diniz B.S.
        • Teixeira A.L.
        • Talib L.L.
        • Mendonca V.A.
        • Gattaz W.F.
        • Forlenza O.V.
        Serum brain-derived neurotrophic factor level is reduced in antidepressant-free patients with late-life depression.
        World J Biol Psychiatry. 2010; 11: 550-555
        • Alexopoulos G.S.
        Depression in the elderly.
        Lancet. 2005; 365: 1961-1970
        • Heikkinen R.L.
        • Kauppinen M.
        Depressive symptoms in late life: a 10-year follow-up.
        Arch Gerontol Geriatr. 2004; 38: 239-250
        • Bus B.A.
        • Tendolkar I.
        • Franke B.
        • et al.
        Serum brain-derived neurotrophic factor: determinants and relationship with depressive symptoms in a community population of middle-aged and elderly people.
        World J Biol Psychiatry. 2012; 13: 39-47
        • Komulainen P.
        • Pedersen M.
        • Hanninen T.
        • et al.
        BDNF is a novel marker of cognitive function in ageing women: the DR's EXTRA Study.
        Neurobiol Learn Mem. 2008; 90: 596-603
        • Krabbe K.S.
        • Mortensen E.L.
        • Avlund K.
        • et al.
        Brain-derived neurotrophic factor predicts mortality risk in older women.
        J Am Geriatr Soc. 2009; 57: 1447-1452
        • Kerse N.
        • Hayman K.J.
        • Moyes S.A.
        • et al.
        Home-based activity program for older people with depressive symptoms: DeLLITE–a randomized controlled trial.
        Ann Fam Med. 2010; 8: 214-223
        • Lampinen P.
        • Heikkinen E.
        Reduced mobility and physical activity as predictors of depressive symptoms among community-dwelling older adults: an eight-year follow-up study.
        Aging Clin Exp Res. 2003; 15: 205-211
        • Cotman C.W.
        • Berchtold N.C.
        Exercise: a behavioral intervention to enhance brain health and plasticity.
        Trends Neurosci. 2002; 25: 295-301
        • Liu-Ambrose T.
        • Donaldson M.G.
        Exercise and cognition in older adults: is there a role for resistance training programmes?.
        Br J Sports Med. 2009; 43: 25-27
        • Coelho F.M.
        • Pereira D.S.
        • Lustosa L.P.
        • et al.
        Physical therapy intervention (PTI) increases plasma brain-derived neurotrophic factor (BDNF) levels in non-frail and pre-frail elderly women.
        Arch Gerontol Geriatr. 2011; 54: 415-420
        • Pedersen B.K.
        • Pedersen M.
        • Krabbe K.S.
        • Bruunsgaard H.
        • Matthews V.B.
        • Febbraio M.A.
        Role of exercise-induced brain-derived neurotrophic factor production in the regulation of energy homeostasis in mammals.
        Exp Physiol. 2009; 94: 1153-1160
        • Ferris L.T.
        • Williams J.S.
        • Shen C.L.
        The effect of acute exercise on serum brain-derived neurotrophic factor levels and cognitive function.
        Med Sci Sports Exerc. 2007; 39: 728-734
        • Gustafsson G.
        • Lira C.M.
        • Johansson J.
        • et al.
        The acute response of plasma brain-derived neurotrophic factor as a result of exercise in major depressive disorder.
        Psychiatry Res. 2009; 169: 244-248
        • Zoladz J.A.
        • Pilc A.
        The effect of physical activity on the brain derived neurotrophic factor: from animal to human studies.
        J Physiol Pharmacol. 2010; 61: 533-541
        • Goekint M.
        • De Pauw K.
        • Roelands B.
        • et al.
        Strength training does not influence serum brain-derived neurotrophic factor.
        Eur J Appl Physiol. 2010; 110: 285-293
        • Levinger I.
        • Goodman C.
        • Matthews V.
        • et al.
        BDNF, metabolic risk factors, and resistance training in middle-aged individuals.
        Med Sci Sports Exerc. 2008; 40: 535-541
        • Yarrow J.F.
        • White L.J.
        • McCoy S.C.
        • Borst S.E.
        Training augments resistance exercise induced elevation of circulating brain derived neurotrophic factor (BDNF).
        Neurosci Lett. 2010; 479: 161-165
        • Kryger A.I.
        • Andersen J.L.
        Resistance training in the oldest old: consequences for muscle strength, fiber types, fiber size, and MHC isoforms.
        Scand J Med Sci Sports. 2007; 17: 422-430
        • Chodzko-Zajko W.J.
        • Proctor D.N.
        • Fiatarone Singh M.A.
        • et al.
        American College of Sports Medicine position stand. Exercise and physical activity for older adults.
        Med Sci Sports Exerc. 2009; 41: 1510-1530
        • Pereira D.S.
        • Queiroz B.Z.
        • Mateo E.C.
        • et al.
        Interaction between cytokine gene polymorphisms and the effect of physical exercise on clinical and inflammatory parameters in older women: study protocol for a randomized controlled trial.
        Trials. 2012; 13: 134
        • Bertolucci P.H.
        • Brucki S.M.
        • Campacci S.R.
        • Juliano Y.
        O Mini-exame do estado mental em uma população geral: impacto da escolaridade.
        Arq Neuropsiquiatr. 1994; 52: 1-7
        • Folstein M.F.
        • Folstein S.E.
        • McHugh P.R.
        Mini-mental state: a practical method for grading the cognitive status of patients for the clinician.
        J Psychiatr Res. 1975; 12: 189-198
        • Yesavage J.A.
        • Brink T.L.
        • Rose T.L.
        • Lum O.
        • Huang V.
        • Adey M.
        Development and validation of a geriatric depression screening scale: a preliminary report.
        J Psychiatr Res. 1982; 17: 37-49
        • Almeida O.P.
        • Almeida S.A.
        Confiabilidade da versão brasileira da Escala de Depressão em Geriatria (GDS) versão reduzida.
        Arq Neuropsiquiatr. 1999; 57: 421-426
        • Lustosa L.P.
        • Silva J.P.
        • Coelho F.M.
        • Pereira D.S.
        • Parentoni A.N.
        • Pereira L.S.
        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.
        Rev Bras Fisioter. 2011; 15: 318-324
        • Drouin J.M.
        • Valovich-McLeod T.C.
        • Shultz S.J.
        • Gansneder B.M.
        • Perrin D.H.
        Reliability and validity of the Biodex system 3 pro isokinetic dynamometer velocity, torque and position measurements.
        Eur J Appl Physiol. 2004; 91: 22-29
        • Enright P.L.
        The six-minute walk test.
        Respir Care. 2003; 48: 783-785
        • Castellano V.
        • White L.J.
        Serum brain-derived neurotrophic factor response to aerobic exercise in multiple sclerosis.
        J Neurol Sci. 2008; 269: 85-91
        • Seifert T.
        • Brassard P.
        • Wissenberg M.
        • et al.
        Endurance training enhances BDNF release from the human brain.
        Am J Physiol Regul Integr Comp Physiol. 2010; 298: R372-R377
        • Erickson K.I.
        • Voss M.W.
        • Prakash R.S.
        • et al.
        Exercise training increases size of hippocampus and improves memory.
        Proc Natl Acad Sci U S A. 2011; 108: 3017-3022
        • Donovan M.J.
        • Lin M.I.
        • Wiegn P.
        • et al.
        Brain derived neurotrophic factor is an endothelial cell survival factor required for intramyocardial vessel stabilization.
        Development. 2000; 127: 4531-4540
        • Nakahashi T.
        • Fujimura H.
        • Altar C.A.
        • et al.
        Vascular endothelial cells synthesize and secrete brain-derived neurotrophic factor.
        FEBS Lett. 2000; 470: 113-117
        • Kerschensteiner M.
        • Gallmeier E.
        • Behrens L.
        • et al.
        Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in inflammatory brain lesions: a neuroprotective role of inflammation?.
        J Exp Med. 1999; 189: 865-870
        • Matthews V.B.
        • Astrom M.B.
        • Chan M.H.
        • et al.
        Brain-derived neurotrophic factor is produced by skeletal muscle cells in response to contraction and enhances fat oxidation via activation of AMP-activated protein kinase.
        Diabetologia. 2009; 52: 1409-1418
        • Neeper S.A.
        • Gomez-Pinilla F.
        • Choi J.
        • Cotman C.W.
        Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain.
        Brain Res. 1996; 726: 49-56
        • Rasmussen P.
        • Brassard P.
        • Adser H.
        • et al.
        Evidence for a release of brain-derived neurotrophic factor from the brain during exercise.
        Exp Physiol. 2009; 94: 1062-1069
        • Carek P.J.
        • Laibstain S.E.
        • Carek S.M.
        Exercise for the treatment of depression and anxiety.
        Int J Psychiatry Med. 2011; 41: 15-28
        • Conn V.S.
        Depressive symptom outcomes of physical activity interventions: meta-analysis findings.
        Ann Behav Med. 2010; 39: 128-138
        • Mead G.E.
        • Morley W.
        • Campbell P.
        • Greig C.A.
        • McMurdo M.
        • Lawlor D.A.
        Exercise for depression.
        Cochrane Database Syst Rev. 2009; : CD004366
        • Sjosten N.
        • Kivela S.L.
        The effects of physical exercise on depressive symptoms among the aged: a systematic review.
        Int J Geriatr Psychiatry. 2006; 21: 410-418
        • Pasco J.A.
        • Williams L.J.
        • Jacka F.N.
        • et al.
        Habitual physical activity and the risk for depressive and anxiety disorders among older men and women.
        Int Psychogeriatr. 2011; 23: 292-298
        • Strawbridge W.J.
        • Deleger S.
        • Roberts R.E.
        • Kaplan G.A.
        Physical activity reduces the risk of subsequent depression for older adults.
        Am J Epidemiol. 2002; 156: 328-334
        • Lawlor D.A.
        • Hopker S.W.
        The effectiveness of exercise as an intervention in the management of depression: systematic review and meta-regression analysis of randomised controlled trials.
        BMJ. 2001; 322: 763-767
        • Martinsen E.W.
        Physical activity and depression: clinical experience.
        Acta Psychiatr Scand Suppl. 1994; 377: 23-27
        • Salmon P.
        Effects of physical exercise on anxiety, depression, and sensitivity to stress: a unifying theory.
        Clin Psychol Rev. 2001; 21: 33-61
        • Archer T.
        • Fredriksson A.
        • Schutz E.
        • Kostrzewa R.M.
        Influence of physical exercise on neuroimmunological functioning and health: aging and stress.
        Neurotox Res. 2011; 20: 69-83
        • Beavers K.M.
        • Brinkley T.E.
        • Nicklas B.J.
        Effect of exercise training on chronic inflammation.
        Clin Chim Acta. 2010; 411: 785-793
        • Churchill J.D.
        • Galvez R.
        • Colcombe S.
        • Swain R.A.
        • Kramer A.F.
        • Greenough W.T.
        Exercise, experience and the aging brain.
        Neurobiol Aging. 2002; 23: 941-955
        • Murrell C.J.
        • Cotter J.D.
        • Thomas K.N.
        • Lucas S.J.E.
        • Williams M.J.A.
        • Ainslie P.N.
        Cerebral blood flow and cerebrovascular reactivity at restand during sub-maximal exercise: effect of age and 12-week exercise training.
        Age (Dordr). 2013; 35: 905-920
        • Aydemir O.
        • Deveci A.
        • Taskin O.E.
        • Taneli F.
        • Esen-Danaci A.
        Serum brain-derived neurotrophic factor level in dysthymia: a comparative study with major depressive disorder.
        Prog Neuropsychopharmacol Biol Psychiatry. 2007; 31: 1023-1026
        • Taylor W.D.
        • Zuchner S.
        • McQuoid D.R.
        • Steffens D.C.
        • Speer M.C.
        • Krishnan K.R.
        Allelic differences in the brain-derived neurotrophic factor Val66Met polymorphism in late-life depression.
        Am J Geriatr Psychiatry. 2007; 15: 850-857
        • Lommatzsch M.
        • Zingler D.
        • Schuhbaeck K.
        • et al.
        The impact of age, weight and gender on BDNF levels in human platelets and plasma.
        Neurobiol Aging. 2005; 26: 115-123
        • Sohrabji F.
        • Lewis D.K.
        Estrogen–BDNF interactions: implications for neurodegenerative diseases.
        Front Neuroendocrinol. 2006; 27: 404-414
        • Paradela E.M.P.
        • Lourenço R.A.
        • Veras R.P.
        Validation of geriatric depression scale in a general outpatient clinic.
        Rev Saúde Pública. 2005; 39: 918-923