The Effect of exercise training on resting concentrations of peripheral brain-derived neurotrophic factor (BDNF): A meta-analysis

PLoS ONE

Volumn 11, Issue 9, 2016, Pages

  Dinoff, Adam ^a,b   Herrmann, Nathan ^a,b   Swardfager, Walter ^a,b   Liu, Celina S ^a,b   Sherman, Chelsea ^a   Chan, Sarah ^a   Lanctôt, Krista L ^a,b  

^a Sunnybrook Health Sciences Centre   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

AEROBIC EXERCISE; ARTICLE; EXERCISE; HUMAN; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PUBLISHING; RESISTANCE TRAINING; REST; SYSTEMATIC REVIEW;

EID: 84993929250     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0163037     Document Type: Article

References (138)

1. Basso JC, Shang A, Elman M, Karmouta R, Suzuki WA. Acute Exercise Improves Prefrontal Cortex but not Hippocampal Function in Healthy Adults. J Int Neuropsychol Soc. 2015; 21(10): 791-801. doi: 10.1017/S135561771500106X PMID: 26581791.
2. Best JR, Chiu BK, Liang Hsu C, Nagamatsu LS, Liu-Ambrose T. Long-Term Effects of Resistance Exercise Training on Cognition and Brain Volume in Older Women: Results from a Randomized Controlled Trial. J Int Neuropsychol Soc. 2015; 21(10): 745-56. doi: 10.1017/S1355617715000673 PMID: 26581787.
3. Bossers WJ, van der Woude LH, Boersma F, Hortobagyi T, Scherder EJ, van Heuvelen MJ. A 9-Week Aerobic and Strength Training Program Improves Cognitive and Motor Function in Patients with Dementia: A Randomized, Controlled Trial. Am J Geriatr Psychiatry. 2015. doi: 10.1016/j.jagp.2014.12.191 PMID: 25648055.
4. Hagovska M, Takac P, Dzvonik O. Effect of a combining cognitive and balanced training on the cognitive postural and functional status of seniors with a mild cognitive deficit in a randomized, controlled trial. Eur J Phys Rehabil Med. 2015. PMID: 26325026.
5. Dauwan M, Begemann MJ, Heringa SM, Sommer IE. Exercise Improves Clinical Symptoms, Quality of Life, Global Functioning, and Depression in Schizophrenia: A Systematic Review and Meta-analysis. Schizophr Bull. 2015. doi: 10.1093/schbul/sbv164 PMID: 26547223.
6. de Souza Moura AM, Lamego MK, Paes F, Rocha NB, Simoes-Silva V, Rocha SA, et al. Effects of aerobic exercise on anxiety disorders: a systematic review. CNS & neurological disorders drug targets. 2015. PMID: 26556089.
7. Kerling A, Tegtbur U, Gutzlaff E, Kuck M, Borchert L, Ates Z, et al. Effects of adjunctive exercise on physiological and psychological parameters in depression: a randomized pilot trial. J Affect Disord. 2015; 177: 1-6. doi: 10.1016/j.jad.2015.01.006 PMID: 25743367.
8. Knapen J, Vancampfort D, Morien Y, Marchal Y. Exercise therapy improves both mental and physical health in patients with major depression. Disabil Rehabil. 2015; 37(16): 1490-5. doi: 10.3109/09638288.2014.972579 PMID: 25342564.
9. Pedersen BK, Saltin B. Exercise as medicine - evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand J Med Sci Sports. 2015; 25 Suppl 3: 1-72. doi: 10.1111/sms.12581 PMID: 26606383.
10. Rethorst CD, Wipfli BM, Landers DM. The Antidepressive Effects of Exercise: A Meta-Analysis of Randomized Trials. Sports Med. 2009; 39(6): 491-511. PMID: 48381815. doi: 10.2165/00007256-200939060-00004
11. Wipfli BM, Rethorst CD, Landers DM. The anxiolytic effects of exercise: a meta-analysis of randomized trials and dose-response analysis. J Sport Exerc Psychol. 2008; 30(4): 392-410. PMID: 18723899.
12. Gligoroska JP, Manchevska S. The effect of physical activity on cognition - physiological mechanisms. Mater. 2012; 24(3): 198-202. http://dx.doi.org/10.5455/msm.2012.24.198-202. PMID: 23678325; PubMed Central PMCID: PMCPMC3633396.
13. Kramer AF, Erickson KI, Colcombe SJ. Exercise, cognition, and the aging brain. J Appl Physiol (1985). 2006; 101(4): 1237-42. doi: 10.1152/japplphysiol.00500.2006 PMID: 16778001.
14. Brosse AL, Sheets ES, Lett HS, Blumenthal JA. Exercise and the treatment of clinical depression in adults: recent findings and future directions. Sports Med. 2002; 32(12): 741-60. PMID: 12238939.
15. Acheson A, Conover JC, Fandl JP, DeChiara TM, Russell M, Thadani A, et al. A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature. 1995; 374(6521): 450-3. doi: 10.1038/374450a0 PMID: 7700353.
16. Greenberg ME, Xu B, Lu B, Hempstead BL. New insights in the biology of BDNF synthesis and release: implications in CNS function. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2009; 29(41): 12764-7. doi: 10.1523/JNEUROSCI.3566-09.2009 PMID: 19828787; PubMed Central PMCID: PMCPMC3091387.
17. Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci. 2001; 24: 677-736. doi: 10.1146/annurev.neuro.24.1.677 PMID: 11520916; PubMed Central PMCID: PMCPMC2758233.
18. Numakawa T, Suzuki S, Kumamaru E, Adachi N, Richards M, Kunugi H. BDNF function and intracellular signaling in neurons. Histol Histopathol. 2010; 25(2): 237-58. PMID: 20017110.
19. Erickson K, Weinstein AM, Verstynen TD, Voss MW, Prakash RS, Woods J, et al. The influence of an aerobic exercise intervention on brain volume in late adulthood. Alzheimer's and Dementia. 2012; 1:): P81. http://dx.doi.org/10.1016/j.jalz.2012.05.197. PMID: 70859421.
20. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA. 2011; 108(7): 3017-22. http://dx.doi.org/10.1073/pnas.1015950108. PMID: 21282661; PubMed Central PMCID: PMCPMC3041121. doi: 10.1073/pnas.1015950108
21. Scharfman H, Goodman J, Macleod A, Phani S, Antonelli C, Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol. 2005; 192 (2): 348-56. doi: 10.1016/j.expneurol.2004.11.016 PMID: 15755552.
22. Tolwani RJ, Buckmaster PS, Varma S, Cosgaya JM, Wu Y, Suri C, et al. BDNF overexpression increases dendrite complexity in hippocampal dentate gyrus. Neuroscience. 2002; 114(3): 795-805. PMID: 12220579.
23. Arancibia S, Silhol M, Mouliere F, Meffre J, Hollinger I, Maurice T, et al. Protective effect of BDNF against beta-amyloid induced neurotoxicity in vitro and in vivo in rats. Neurobiol Dis. 2008; 31(3): 316-26. doi: 10.1016/j.nbd.2008.05.012 PMID: 18585459.
24. M Q. Beneficial effects of moderate voluntary physical exercise and its biological mechanisms on brain health. Neurosci Bull. 2008; 24(4): 265-70. doi: 10.1007/s12264-008-0402-1 PMID: 18668156
25. Cotman CW, Berchtold NC. Physical activity and the maintenance of cognition: learning from animal models. Alzheimer's & dementia: the journal of the Alzheimer's Association. 2007; 3(2 Suppl): S30-7. doi: 10.1016/j.jalz.2007.01.013 PMID: 19595972.
26. Fernandes BS, Molendijk ML, Kohler CA, Soares JC, Leite CM, Machado-Vieira R, et al. Peripheral brain-derived neurotrophic factor (BDNF) as a biomarker in bipolar disorder: a meta-analysis of 52 studies. BMC Med. 2015; 13: 289. doi: 10.1186/s12916-015-0529-7 PMID: 26621529; PubMed Central PMCID: PMCPMC4666054.
27. Polyakova M, Stuke K, Schuemberg K, Mueller K, Schoenknecht P, Schroeter ML. BDNF as a biomarker for successful treatment of mood disorders: a systematic & quantitative meta-analysis. J Affect Disord. 2015; 174: 432-40. doi: 10.1016/j.jad.2014.11.044 PMID: 25553404.
28. Molendijk ML, Spinhoven P, Polak M, Bus BA, Penninx BW, Elzinga BM. Serum BDNF concentrations as peripheral manifestations of depression: evidence from a systematic review and meta-analyses on 179 associations (N = 9484). Mol Psychiatry. 2014; 19(7): 791-800. doi: 10.1038/mp.2013.105 PMID: 23958957.
29. Fernandes BS, Steiner J, Berk M, Molendijk ML, Gonzalez-Pinto A, Turck CW, et al. Peripheral brain-derived neurotrophic factor in schizophrenia and the role of antipsychotics: meta-analysis and implications. Mol Psychiatry. 2015; 20(9): 1108-19. doi: 10.1038/mp.2014.117 PMID: 25266124.
30. Green MJ, Matheson SL, Shepherd A, Weickert CS, Carr VJ. Brain-derived neurotrophic factor levels in schizophrenia: a systematic review with meta-analysis. Mol Psychiatry. 2011; 16(9): 960-72. doi: 10.1038/mp.2010.88 PMID: 20733577.
31. Suliman S, Hemmings SM, Seedat S. Brain-Derived Neurotrophic Factor (BDNF) protein levels in anxiety disorders: systematic review and meta-regression analysis. Front Integr Neurosci. 2013; 7: 55. doi: 10.3389/fnint.2013.00055 PMID: 23908608; PubMed Central PMCID: PMCPMC3725410.
32. Libman-Sokolowska M, Drozdowicz E, Nasierowski T. BDNF as a biomarker in the course and treatment of schizophrenia. Psychiatr Pol. 2015; 49(6): 1149-58. doi: 10.12740/PP/37705 PMID: 26909392.
33. Krabbe KS, Nielsen AR, Krogh-Madsen R, Plomgaard P, Rasmussen P, Erikstrup C, et al. Brain-derived neurotrophic factor (BDNF) and type 2 diabetes. Diabetologia. 2007; 50(2): 431-8. doi: 10.1007/s00125-006-0537-4 PMID: 17151862.
34. Wens I, Keytsmen C, Dalgas U, Eijinde BO. The impact of 24 weeks combined exercise on BDNF expression in relapsing-remitting multiple sclerosis patients. Annual Rehabilitation in Multiple Sclerosis Conference. 2015; 21(4): 533-4.
35. Tonoli C, Heyman E, Roelands B, Buyse L, Piacentini F, Berthoin S, et al. BDNF, IGF-I, Glucose and Insulin during Continuous and Interval Exercise in Type 1 Diabetes. Int J Sports Med. 2015; 36 (12): 955-9. doi: 10.1055/s-0035-1548886 PMID: 26212245.
36. Schuch FB, da Silveira LE, de Zeni TC, da Silva DP, Wollenhaupt-Aguiar B, Ferrari P, et al. Effects of a single bout of maximal aerobic exercise on BDNF in bipolar disorder: A gender-based response. Psychiatry Res. 2015; 229(1-2): 57-62. doi: 10.1016/j.psychres.2015.07.072 PMID: 26239767.
37. Nascimento CM, Pereira JR, Pires de andrade L, Garuffi M, Ayan C, Kerr DS, et al. Physical exercise improves peripheral BDNF levels and cognitive functions in mild cognitive impairment elderly with different bdnf Val66Met genotypes. J Alzheimers Dis. 2015; 43(1): 81-91. doi: 10.3233/JAD-140576 PMID: 25062900.
38. Zoladz JA, Majerczak J, Zeligowska E, Mencel J, Jaskolski A, Jaskolska A, et al. Moderate-intensity interval training increases serum brain-derived neurotrophic factor level and decreases inflammation in parkinson's disease patients. Journal of Physiology and Pharmacology. 2014; 65(3): 441-8. PMID: 2014407145.
39. Leckie RL, Oberlin LE, Voss MW, Prakash RS, Szabo-Reed A, Chaddock-Heyman L, et al. BDNF mediates improvements in executive function following a 1-year exercise intervention. Frontiers in human neuroscience. 2014; 8: 985. doi: 10.3389/fnhum.2014.00985 PMID: 25566019; PubMed Central PMCID: PMC4263078.
40. Schmolesky MT, Webb DL, Hansen RA. The effects of aerobic exercise intensity and duration on levels of brain-derived neurotrophic factor in healthy men. J Sports Sci Med. 2013; 12(3): 502-11. PMID: 24149158; PubMed Central PMCID: PMCPMC3772595.
41. Araya AV, Orellana X, Godoy D, Soto L, Fiedler J. Effect of exercise on circulating levels of brain-derived neurotrophic factor (BDNF) in overweight and obese subjects. Horm Metab Res. 2013; 45 (7): 541-4. http://dx.doi.org/10.1055/s-0032-1333237. PMID: 23386418. doi: 10.1055/s-0032-1333237
42. Berchtold NC, Adlard PA, Kesslak JP, Pike CJ, Cotman CW. Hippocampal BDNF protein is increased by exercise and estrogen. Society for Neuroscience Abstracts. 2001; 27(1): 280-. PMID: BCI: BCI200100478265.
43. Koo JH, Kwon IS, Kang EB, Lee CK, Lee NH, Kwon MG, et al. Neuroprotective effects of treadmill exercise on BDNF and PI3-K/Akt signaling pathway in the cortex of transgenic mice model of Alzheimer's disease. Journal of exercise nutrition & biochemistry. 2013; 17(4): 151-60. doi: 10.5717/jenb.2013.17.4.151 PMID: 25566426; PubMed Central PMCID: PMC4241914.
44. Geng YM, Yu F, Wang Z. Effect of Exercise on BDNF, HSP70, and Oxidative Stress Level in Prefrontal Cortex of Depression Rat. Journal of Xi'an Institute of Physical Education. 2013; 30(4): 448-52, 58. PMID: 1443379837; 18671602.
45. Groves-Chapman JL, Murray PS, Stevens KL, Monroe DC, Koch LG, Britton SL, et al. Changes in mRNA levels for brain-derived neurotrophic factor after wheel running in rats selectively bred for highand low-aerobic capacity. Brain Res. 2011; 1425: 90-7. http://dx.doi.org/10.1016/j.brainres.2011.09.059. PMID: 911166870; 16058287. doi: 10.1016/j.brainres.2011.09.059
46. Gustafsson S, Liang W, Hilke S. Effects of voluntary running in the female mice lateral septum on BDNF and corticotropin-releasing factor receptor 2. Int J Pept. 2011; 2011: 932361. http://dx.doi.org/10.1155/2011/932361. PMID: 21977046; PubMed Central PMCID: PMCPMC3184426. doi: 10.1155/2011/932361
47. Klintsova AY, Dickson E, Yoshida R, Greenough WT. Altered expression of BDNF and its high-affinity receptor TrkB in response to complex motor learning and moderate exercise. Brain Res. 2004; 1028 (1): 92-104. http://dx.doi.org/10.1016/j.brainres.2004.09.003.
48. Fang Z, Lee C, Seo M, Cho H, Lee J, Lee B, et al. Effect of treadmill exercise on the BDNF-mediated pathway in the hippocampus of stressed rats. Neuroscience Research. 2013; 76(1-2): 187-94. http://dx.doi.org/10.1016/j.neures.2013.04.005. PMID: 1500774116; 19260602.
49. Liu YF, Chen HI, Wu CL, Kuo YM, Yu L, Huang AM, et al. Differential effects of treadmill running and wheel running on spatial or aversive learning and memory: Roles of amygdalar brain-derived neurotrophic factor and synaptotagmin I. J Physiol (Lond). 2009; 587(13): 3221-31. http://dx.doi.org/10.1113/jphysiol.2009.173088. PMID: 2009348033.
50. Lu J, Xu Y, Hu W, Gao Y, Ni X, Sheng H, et al. Exercise ameliorates depression-like behavior and increases hippocampal BDNF level in ovariectomized rats. Neurosci Lett. 2014; 573: 13-8. http://dx.doi.org/10.1016/j.neulet.2014.04.053. PMID: 24813109. doi: 10.1016/j.neulet.2014.04.053
51. Marais L, Stein DJ, Daniels WMU Exercise increases BDNF levels in the striatum and decreases depressive-like behavior in chronically stressed rats. Metabolic Brain Disease. 2009; 24(4): 587-97. http://dx.doi.org/10.1007/s11011-009-9157-2. PMID: 19844781; 11893486. doi: 10.1007/s11011-009-9157-2
52. Marlatt MW, Potter MC, Lucassen PJ, van Praag H. Running throughout middle-age improves memory function, hippocampal neurogenesis, and BDNF levels in female C57BL/6J mice. Developmental Neurobiology. 2012; 72(6): 943-52. doi: 10.1002/dneu.22009 PMID: WOS:000303985400016.
53. Mojtahedi S, Kordi MR, Hosseini SE, Omran SF, Soleimani M. Effect of treadmill running on the expression of genes that are involved in neuronal differentiation in the hippocampus of adult male rats. Cell Biology International. 2013; 37(4): 276-83. doi: 10.1002/cbin.10022 PMID: WOS:000316222000002.
54. Neeper SA, Gomez-Pinilla F, Choi J, Cotman C. Physical activity up-regulates BDNF and NGF mRNAin the rat brain. Society for Neuroscience Abstracts. 1995; 21(1-3): 296-. PMID: BCI: BCI199598441729.
55. Pedroso J, Chadi G. Effects of Spontaneous Running in mRNA BDNF Expression in Rat Hippocampus and in Anxiety and Memory Responses Through an Elevated T-Maze. Motor Control. 2007; 11: 1. PMID: 20903834; 7553429.
56. Neeper SA, GomezPinilla F, Choi J, Cotman CW. Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res. 1996; 726(1-2): 49-56. doi: 10.1016/s0006-8993(96)00273-9 PMID: WOS:A1996UZ32300006.
57. Currie J, Ramsbottom R, Gilder M. Serum and plasma concentrations of brain derived neurotrophic factor in response to maximal exercise. J Sports Sci Med. 2009; 8. PMID: 754902573; 13551504.
58. Damirchi A, Tehrani BS, Alamdari KA, Babaei P. Influence of aerobic training and detraining on serum BDNF, insulin resistance, and metabolic risk factors in middle-aged men diagnosed with metabolic syndrome. Clin J Sport Med. 2014; 24(6): 513-8. doi: 10.1097/JSM.0000000000000082 PMID: 24662570.
59. Ferris LT, Williams JS, Shen C-L. Serum Neurotrophin Levels Following Acute Exercise In Humans. Medicine and Science in Sports and Exercise. 2005; 37:S108-S. doi: 10.1097/00005768-200505001-00565 PMID: WOS:000208070300429.
60. Forti LN, Njemini R, Beyer I, Eelbode E, Meeusen R, Mets T, et al. Strength training reduces circulating interleukin-6 but not brain-derived neurotrophic factor in community-dwelling elderly individuals. Age (Dordr). 2014; 36(5): 9704. http://dx.doi.org/10.1007/s11357-014-9704-6. PMID: 25128203.
61. Goekint M, De Pauw K, Roelands B, Njemini R, Bautmans I, Mets T, et al. Strength training does not influence serum brain-derived neurotrophic factor. Eur J Appl Physiol. 2010; 110(2): 285-93. http://dx.doi.org/10.1007/s00421-010-1461-3. PMID: 20467874. doi: 10.1007/s00421-010-1461-3
62. Gomes WF, Lacerda AC, Mendonca VA, Arrieiro AN, Fonseca SF, Amorim MR, et al. Effect of exercise on the plasma BDNF levels in elderly women with knee osteoarthritis. Rheumatol Int. 2014; 34 (6): 841-6. http://dx.doi.org/10.1007/s00296-013-2786-0. PMID: 23739920. doi: 10.1007/s00296-013-2786-0
63. Griffin EW, Mullally S, Foley C, Warmington SA, O'Mara SM, Kelly AM. Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol Behav. 2011; 104(5): 934-41. http://dx.doi.org/10.1016/j.physbeh.2011.06.005. PMID: 21722657. doi: 10.1016/j.physbeh.2011.06.005
64. Toups MS, Greer TL, Kurian BT, Grannemann BD, Carmody TJ, Huebinger R, et al. Effects of serum Brain Derived Neurotrophic Factor on exercise augmentation treatment of depression. J Psychiatr Res. 2011; 45(10): 1301-6. http://dx.doi.org/10.1016/j.jpsychires.2011.05.002. PMID: 21641002. doi: 10.1016/j.jpsychires.2011.05.002
65. Baker LD, Frank LL, Foster-Schubert K, Green PS, Wilkinson CW, McTiernan A, et al. Aerobic exercise improves cognition for older adults with glucose intolerance, a risk factor for Alzheimer's disease. J Alzheimers Dis. 2010; 22(2): 569-79. http://dx.doi.org/10.3233/JAD-2010-100768. PMID: 20847403; PubMed Central PMCID: PMCNIHMS267530PMC3049111. doi: 10.3233/JAD-2010-100768
66. Baker LD, Frank LL, Foster-Schubert K, Green PS, Wilkinson CW, McTiernan A, et al. Effects of aerobic exercise on mild cognitive impairment: A controlled trial. Archives of Neurology. 2010; 67(1): 71-9. http://dx.doi.org/10.1001/archneurol.2009.307. PMID: 2010062777. doi: 10.1001/archneurol.2009.307
67. Pareja-Galeano H, Alis R, Sanchis-Gomar F, Cabo H, Cortell-Ballester J, Gomez-Cabrera MC, et al. Methodological considerations to determine the effect of exercise on brain-derived neurotrophic factor levels. Clin Biochem. 2015; 48(3): 162-6. doi: 10.1016/j.clinbiochem.2014.11.013 PMID: 25464018.
68. Huang T, Larsen KT, Ried-Larsen M, Moller NC, Andersen LB. The effects of physical activity and exercise on brain-derived neurotrophic factor in healthy humans: a review. Scand J Med Sci Sports. 2014; 24(1): 1-10. http://dx.doi.org/10.1111/sms.12069. PMID: 23600729. doi: 10.1111/sms.12069
69. Knaepen K, Goekint M, Heyman EM, Meeusen R. Neuroplasticity - Exercise-Induced Response of Peripheral Brain-Derived Neurotrophic Factor: A Systematic Review of Experimental Studies in Human Subjects. Sports Med. 2010; 40(9): 765-801. PMID: 55274657. doi: 10.2165/11534530-000000000-00000
70. Zoladz JA, Pilc A. The effect of physical activity on the brain derived neurotrophic factor: from animal to human studies. J Physiol Pharmacol. 2010; 61(5): 533-41. PMID: 21081796.
71. Coelho FGDM, Gobbi S, Andreatto CAA, Corazza DI, Pedroso RV, Santos-Galduroz RF. Physical exercise modulates peripheral levels of brain-derived neurotrophic factor (BDNF): A systematic review of experimental studies in the elderly. Archives of Gerontology and Geriatrics. 2013; 56(1): 10-5. http://dx.doi.org/10.1016/j.archger.2012.06.003. PMID: 2012682428. doi: 10.1016/j.archger.2012.06.003
72. Szuhany KL, Bugatti M, Otto MW. A meta-analytic review of the effects of exercise on brain-derived neurotrophic factor. J Psychiatr Res. 2015; 60: 56-64. doi: 10.1016/j.jpsychires.2014.10.003 PMID: 25455510; PubMed Central PMCID: PMC4314337.
73. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med. 2009; 6(7): e1000100. doi: 10.1371/journal.pmed.1000100 PMID: 19621070; PubMed Central PMCID: PMCPMC2707010.
74. Henning PC, Scofield DE, Spiering BA, Staab JS, Matheny RW Jr, Smith MA, et al. Recovery of endocrine and inflammatory mediators following an extended energy deficit. Journal of Clinical Endocrinology and Metabolism. 2014; 99(3): 956-64. http://dx.doi.org/10.1210/jc.2013-3046. PMID: 2014169269. doi: 10.1210/jc.2013-3046
75. Iughetti L, Casarosa E, Predieri B, Patianna V, Luisi S. Plasma brain-derived neurotrophic factor concentrations in children and adolescents. Neuropeptides. 2011; 45(3): 205-11. doi: 10.1016/j.npep.2011.02.002 PMID: 21420165.
76. Karege F, Perret G, Bondolfi G, Schwald M, Bertschy G, Aubry JM. Decreased serum brain-derived neurotrophic factor levels in major depressed patients. Psychiatry Res. 2002; 109(2): 143-8. doi: 10.1016/s0165-1781(02)00005-7 PMID: WOS:000175506400005.
77. Palomino A, Vallejo-Illarramendi A, Gonzalez-Pinto A, Aldama A, Gonzalez-Gomez C, Mosquera F, et al. Decreased levels of plasma BDNF in first-episode schizophrenia and bipolar disorder patients. Schizophr Res. 2006; 86(1-3): 321-2. doi: 10.1016/j.schres.2006.05.028 PMID: 16829047.
78. Connor B, Young D, Yan Q, Faull RL, Synek B, Dragunow M. Brain-derived neurotrophic factor is reduced in Alzheimer's disease. Brain Res Mol Brain Res. 1997; 49(1-2): 71-81. PMID: 9387865.
79. Frota ER, Rodrigues DH, Donadi EA, Brum DG, Maciel DR, Teixeira AL. Increased plasma levels of brain derived neurotrophic factor (BDNF) after multiple sclerosis relapse. Neurosci Lett. 2009; 460 (2): 130-2. doi: 10.1016/j.neulet.2009.05.057 PMID: 19477225.
80. Fitness NCoS. Relationship between Percent HR Max and Percent VO2 Max.
81. Harris RJ, Bradburn MJ, Deeks JJ, Harbord RM, Altman DG, Sterne JAC metan: fixed- and random-effects meta-analysis. The Stata Journal. 2008; 8(1): 3-28.
82. Noble JE, Wang L, Cerasoli E, Knight AE, Porter RA, Gray E, et al. An international comparability study to determine the sources of uncertainty associated with a non-competitive sandwich fluorescent ELISA. Clin Chem Lab Med. 2008; 46(7): 1033-45. doi: 10.1515/CCLM.2008.182 PMID: 18605964.
83. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002; 21 (11): 1539-58. doi: 10.1002/sim.1186 PMID: 12111919.
84. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997; 315(7109): 629-34. PMID: 9310563; PubMed Central PMCID: PMCPMC2127453.
85. Swardfager W, Herrmann N, Cornish S, Mazereeuw G, Marzolini S, Sham L, et al. Exercise intervention and inflammatory markers in coronary artery disease: a meta-analysis. Am Heart J. 2012; 163 (4): 666-76 e1-3. doi: 10.1016/j.ahj.2011.12.017 PMID: 22520533.
86. Babaei P, Alamdari KA, Tehrani BS, Damirchi A. Effect of six weeks of endurance exercise and following detraining on serum brain derived neurotrophic factor and memory performance in middle aged males with metabolic syndrome. Journal of Sports Medicine and Physical Fitness. 2013; 53 (4): 437-43. PMID: WOS:000324901400011.
87. Bos I, De Boever P, Vanparijs J, Pattyn N, Panis LI, Meeusen R. Subclinical effects of aerobic training in urban environment. Med Sci Sports Exerc. 2013; 45(3): 439-47. http://dx.doi.org/10.1249/MSS.0b013e31827767fc. PMID: 23073213. doi: 10.1249/MSS.0b013e31827767fc
88. Cho HC, Kim JK, Lee NJ, Kim SY, Yoon NK. Effects of combined exercise on cardiovascular risk factors and serum BDNF level in mid-aged women. Journal of exercise nutrition & biochemistry. 2014; 18(1): 61-7. doi: 10.5717/jenb.2014.18.1.61 PMID: 25566440; PubMed Central PMCID: PMC4241931.
89. Coelho FM, Pereira DS, Lustosa LP, Silva JP, Dias JM, Dias RC, 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. 2012; 54(3): 415-20. http://dx.doi.org/10.1016/j.archger.2011.05.014. PMID: 21684022. doi: 10.1016/j.archger.2011.05.014
90. Ferris LT, Williams JS, Akerhielm TD, Hale KB, Parsons SM, Jordan SL, et al. Serum Brain-Derived Neurotrophic Factor Responses to Chronic Exercise Training. Medicine and Science in Sports and Exercise. 2006; 38(5): S522-S3. PMID: WOS:000208070803578.
91. Forti LN, Van Roie E, Njemini R, Coudyzer W, Beyer I, Delecluse C, et al. Dose-and gender-specific effects of resistance training on circulating levels of brain derived neurotrophic factor (BDNF) in community-dwelling older adults. Exp Gerontol. 2015; 70: 144-9. doi: 10.1016/j.exger.2015.08.004 PMID: 26297701.
92. Fragala MS, Beyer KS, Jajtner AR, Townsend JR, Pruna GJ, Boone CH, et al. Resistance exercise may improve spatial awareness and visual reaction in older adults. J Strength Cond Res. 2014; 28 (8): 2079-87. http://dx.doi.org/10.1519/JSC.0000000000000520. PMID: 24832975. doi: 10.1519/JSC.0000000000000520
93. Gapin JI, Wooten JS, Bohall SC, Stout JJ, Smith B, Kirk EP. Associations Between Cognition, Weight Loss, and BDNF Following Exercise Training in Overweight and Obese Adults. Medicine and Science in Sports and Exercise. 2013; 45(5): 559-. PMID: WOS:000330469704272.
94. Goekint M, Roelands B, De Pauw K, Knaepen K, Bos I, Meeusen R. Does a period of detraining cause a decrease in serum brain-derived neurotrophic factor? Neurosci Lett. 2010; 486(3): 146-9. http://dx.doi.org/10.1016/j.neulet.2010.09.032. PMID: 20854879. doi: 10.1016/j.neulet.2010.09.032
95. Kim H, Suzuki T, Kim M, Kojima N, Ota N, Shimotoyodome A, et al. Effects of Exercise and Milk Fat Globule Membrane (MFGM) Supplementation on Body Composition, Physical Function, and Hematological Parameters in Community-Dwelling Frail Japanese Women: A Randomized Double Blind, Placebo-Controlled, Follow-Up Trial. PLoS ONE. 2015; 10(2): e0116256. doi: 10.1371/journal.pone.0116256 PMID: 25659147; PubMed Central PMCID: PMC4319727.
96. Kim Y. The effect of regular Taekwondo exercise on Brain-derived neurotrophic factor and Stroop test in undergraduate student. Journal of exercise nutrition & biochemistry. 2015; 19(2): 73-9. doi: 10.5717/jenb.2015.15060904 PMID: 26244125; PubMed Central PMCID: PMCPMC4523808.
97. Koichiro A, Yusuke O, Shogo T, Shiori H, Fuminori K, Hiroyuki I, et al. Association of serum BDNF concentration with high-intensity interval training. Japanese Journal of Physical Fitness & Sports Medicine. 2015; 64(2): 227-32.
98. Lemos JR Jr., Alves CR, de Souza SB, Marsiglia JD, Silva MS, Pereira AC, et al. Peripheral vascular reactivity and serum BDNF responses to aerobic training are impaired by the BDNF Val66Met polymorphism. Physiol Genomics. 2016; 48(2): 116-23. doi: 10.1152/physiolgenomics.00086.2015 PMID: 26603150.
99. Levinger I, Goodman C, Matthews V, Hare DL, Jerums G, Garnham A, et al. BDNF, metabolic risk factors, and resistance training in middle-aged individuals. Med Sci Sports Exerc. 2008; 40(3): 535-41. http://dx.doi.org/10.1249/MSS.0b013e31815dd057. PMID: 18379218. doi: 10.1249/MSS.0b013e31815dd057
100. Mueller K, Moller HE, Horstmann A, Busse F, Lepsien J, Bluher M, et al. Physical exercise in overweight to obese individuals induces metabolic- and neurotrophic-related structural brain plasticity. Frontiers in human neuroscience. 2015; 9: 372. doi: 10.3389/fnhum.2015.00372 PMID: 26190989; PubMed Central PMCID: PMCPMC4486867.
101. Murawska-Cialowicz E, Wojna J, Zuwala-Jagiello J. Crossfit training changes brain-derived neurotrophic factor and irisin levels at rest, after wingate and progressive tests, and improves aerobic capacity and body composition of young physically active men and women. J Physiol Pharmacol. 2015; 66(6): 811-21. PMID: 26769830.
102. Prestes J, da Cunha Nascimento D, Tibana RA, Teixeira TG, Vieira DC, Tajra V, et al. Understanding the individual responsiveness to resistance training periodization. Age (Dordr). 2015; 37(3): 9793. doi: 10.1007/s11357-015-9793-x PMID: 25971877.
103. Ruiz JR, Gil-Bea F, Bustamante-Ara N, Rodriguez-Romo G, Fiuza-Luces C, Serra-Rexach JA, et al. Resistance training does not have an effect on cognition or related serum biomarkers in nonagenarians: a randomized controlled trial. Int J Sports Med. 2015; 36(1): 54-60. doi: 10.1055/s-0034-1375693 PMID: 25329433.
104. Schiffer T, Schulte S, Hollmann W, Bloch W, Struder HK. Effects of strength and endurance training on brain-derived neurotrophic factor and insulin-like growth factor 1 in humans. Horm Metab Res. 2009; 41(3): 250-4. http://dx.doi.org/10.1055/s-0028-1093322. PMID: 18975254. doi: 10.1055/s0028-1093322
105. Seifert T, Brassard P, Wissenberg M, Rasmussen P, Nordby P, Stallknecht B, et al. Endurance training enhances BDNF release from the human brain. Am J Physiol Regul Integr Comp Physiol. 2010; 298(2): R372-7. http://dx.doi.org/10.1152/ajpregu.00525.2009. PMID: 19923361. doi: 10.1152/ajpregu.00525.2009
106. Wagner G, Herbsleb M, Cruz Fde L, Schumann A, Brunner F, Schachtzabel C, et al. Hippocampal structure, metabolism, and inflammatory response after a 6-week intense aerobic exercise in healthy young adults: a controlled trial. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism. 2015; 35(10): 1570-8. doi: 10.1038/jcbfm.2015.125 PMID: 26082010; PubMed Central PMCID: PMCPMC4640322.
107. Williams JS, Ferris LT. Effects of Endurance Exercise Training on Brain-Derived Neurotrophic Factor. Journal of Exercise Physiology. 2012; 15(4): 11-7. PMID: 1315621576; 17706373.
108. Yarrow JF, White LJ, McCoy SC, Borst SE. Training augments resistance exercise induced elevation of circulating brain derived neurotrophic factor (BDNF). Neurosci Lett. 2010; 479(2): 161-5. http://dx.doi.org/10.1016/j.neulet.2010.05.058. PMID: 20553806. doi: 10.1016/j.neulet.2010.05.058
109. Zoladz JA, Pilc A, Majerczak J, Grandys M, Zapart-Bukowska J, Duda K. Endurance training increases plasma brain-derived neurotrophic factor concentration in young healthy men. J Physiol Pharmacol. 2008; 59 Suppl 7: 119-32. PMID: 19258661.
110. Cohen J. Statistical Power Analysis for the Behavioral Sciences. 2nd ed. Hillsdale, NJ: Erlbaum; 1988.
111. Marais L, Stein DJ, Daniels WM. Exercise increases BDNF levels in the striatum and decreases depressive-like behavior in chronically stressed rats. Metab Brain Dis. 2009; 24(4): 587-97. doi: 10.1007/s11011-009-9157-2 PMID: 19844781.
112. Laske C, Banschbach S, Stransky E, Bosch S, Straten G, Machann J, et al. Exercise-induced normalization of decreased BDNF serum concentration in elderly women with remitted major depression. Int J Neuropsychopharmcol. 2010; 13(5): 595-602. http://dx.doi.org/10.1017/S1461145709991234. PMID: 746083015; 12928638.
113. Heijnen S, Hommel B, Kibele A, Colzato LS. Neuromodulation of Aerobic Exercise-A Review. Front Psychol. 2015; 6: 1890. doi: 10.3389/fpsyg.2015.01890 PMID: 26779053; PubMed Central PMCID: PMCPMC4703784.
114. Catalan-Matamoros D, Gomez-Conesa A, Stubbs B, Vancampfort D. Exercise improves depressive symptoms in older adults: An umbrella review of systematic reviews and meta-analyses. Psychiatry Res. 2016; 244: 202-9. doi: 10.1016/j.psychres.2016.07.028 PMID: 27494042.
115. Laurin D, Verreault R, Lindsay J, MacPherson K, Rockwood K. Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch Neurol. 2001; 58(3): 498-504. PMID: 11255456.
116. Cotman CW, Berchtold NC, Christie LA. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci. 2007; 30(9): 464-72. doi: 10.1016/j.tins.2007.06.011 PMID: 17765329.
117. Fujimura H, Altar CA, Chen R, Nakamura T, Nakahashi T, Kambayashi J, et al. Brain-derived neurotrophic factor is stored in human platelets and released by agonist stimulation. Thromb Haemost. 2002; 87(4): 728-34. PMID: 12008958.
118. Lommatzsch M, Zingler D, Schuhbaeck K, Schloetcke K, Zingler C, Schuff-Werner P, et al. The impact of age, weight and gender on BDNF levels in human platelets and plasma. Neurobiol Aging. 2005; 26(1): 115-23. doi: 10.1016/j.neurobiolaging.2004.03.002 PMID: 15585351.
119. Gomez-Pinilla F, Vaynman S, Ying Z. Brain-derived neurotrophic factor functions as a metabotrophin to mediate the effects of exercise on cognition. Eur J Neurosci. 2008; 28(11): 2278-87. http://dx.doi.org/10.1111/j.1460-9568.2008.06524.x. PMID: 19046371; 8821297. doi: 10.1111/j.1460-9568.2008.06524.x
120. Klein AB, Williamson R, Santini MA, Clemmensen C, Ettrup A, Rios M, et al. Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int J Neuropsychopharmacol. 2011; 14 (3): 347-53. doi: 10.1017/S1461145710000738 PMID: 20604989.
121. Pillai A, Kale A, Joshi S, Naphade N, Raju MS, Nasrallah H, et al. Decreased BDNF levels in CSF of drug-naive first-episode psychotic subjects: correlation with plasma BDNF and psychopathology. Int J Neuropsychopharmacol. 2010; 13(4): 535-9. doi: 10.1017/S1461145709991015 PMID: 19941699.
122. Angelucci F, Gelfo F, De Bartolo P, Caltagirone C, Petrosini L. BDNF concentrations are decreased in serum and parietal cortex in immunotoxin 192 IgG-Saporin rat model of cholinergic degeneration. Neurochem Int. 2011; 59(1): 1-4. doi: 10.1016/j.neuint.2011.04.010 PMID: 21672569.
123. Karege F, Schwald M, Cisse M. Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets. Neurosci Lett. 2002; 328(3): 261-4. PMID: 12147321.
124. Swardfager W, Herrmann N, Marzolini S, Saleem M, Shammi P, Oh P, et al. Brain derived neurotrophic factor, cardiopulmonary fitness and cognition in patients with coronary artery disease. Brain, Behavior, and Immunity. 2011; 25(6): 1264-71. http://dx.doi.org/10.1016/j.bbi.2011.04.017. PMID: 2011-15428-026. doi: 10.1016/j.bbi.2011.04.017
125. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. Exercise training increases size of hippocampus and improves memory. PNAS Proceedings of the National Academy of Sciences of the United States of America. 2011; 108(7): 3017-22. http://dx.doi.org/10.1073/pnas.1015950108. PMID: 2011-06020-007.
126. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. Exercise training increases size of hippocampus and improves memory. Proceedings of the National Academy of Sciences, USA. 2011; 108(7): 3017-22. PMID: 907155834; 14388032.
127. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA. 2011; 108(7): 3017-22. http://dx.doi.org/10.1073/pnas.1015950108. PMID: 2011146091. doi: 10.1073/pnas.1015950108
128. Syvanen S, Lindhe O, Palner M, Kornum BR, Rahman O, Langstrom B, et al. Species differences in blood-brain barrier transport of three positron emission tomography radioligands with emphasis on P-glycoprotein transport. Drug Metab Dispos. 2009; 37(3): 635-43. doi: 10.1124/dmd.108.024745 PMID: 19047468.
129. Lacombe O, Videau O, Chevillon D, Guyot AC, Contreras C, Blondel S, et al. In vitro primary human and animal cell-based blood-brain barrier models as a screening tool in drug discovery. Mol Pharm. 2011; 8(3): 651-63. doi: 10.1021/mp1004614 PMID: 21438632.
130. Vanevski F, Xu B. Molecular and neural bases underlying roles of BDNF in the control of body weight. Front Neurosci. 2013; 7: 37. doi: 10.3389/fnins.2013.00037 PMID: 23519010; PubMed Central PMCID: PMCPMC3604627.
131. Ono M, Ichihara J, Nonomura T, Itakura Y, Taiji M, Nakayama C, et al. Brain-derived neurotrophic factor reduces blood glucose level in obese diabetic mice but not in normal mice. Biochem Biophys Res Commun. 1997; 238(2): 633-7. doi: 10.1006/bbrc.1997.7220 PMID: 9299565.
132. Lommatzsch M, Braun A, Mannsfeldt A, Botchkarev VA, Botchkareva NV, Paus R, et al. Abundant production of brain-derived neurotrophic factor by adult visceral epithelia. Implications for paracrine and target-derived Neurotrophic functions. Am J Pathol. 1999; 155(4): 1183-93. doi: 10.1016/S0002-9440(10)65221-2 PMID: 10514401; PubMed Central PMCID: PMCPMC1867012.
133. Lemos J Jr., De Souza S, Ribeiro R Jr., Dias R, Silva M, Alves C, et al. Aerobic exercise increases parasympathetic activity on BDNF genetic variant Val66Met carriers. FASEB Journal. 2015.
134. Arija V, Ferrer-Barcala M, Aranda N, Canals J. BDNF Val66Met polymorphism, energy intake and BMI: a follow-up study in schoolchildren at risk of eating disorders. BMC Public Health. 2010; 10: 363. doi: 10.1186/1471-2458-10-363 PMID: 20573217; PubMed Central PMCID: PMCPMC2904274.
135. Lang UE, Hellweg R, Sander T, Gallinat J. The Met allele of the BDNF Val66Met polymorphism is associated with increased BDNF serum concentrations. Mol Psychiatry. 2009; 14(2): 120-2. doi: 10.1038/mp.2008.80 PMID: 19156154.
136. Petryshen TL, Sabeti PC, Aldinger KA, Fry B, Fan JB, Schaffner SF, et al. Population genetic study of the brain-derived neurotrophic factor (BDNF) gene. Mol Psychiatry. 2010; 15(8): 810-5. doi: 10.1038/mp.2009.24 PMID: 19255578; PubMed Central PMCID: PMCPMC2888876.
137. Canivet A, Albinet CT, Andre N, Pylouster J, Rodriguez-Ballesteros M, Kitzis A, et al. Effects of BDNF polymorphism and physical activity on episodic memory in the elderly: a cross sectional study. Eur Rev Aging Phys Act. 2015; 12: 15. doi: 10.1186/s11556-015-0159-2 PMID: 26865879; PubMed Central PMCID: PMCPMC4748321.
138. Kang HJ, Bae KY, Kim SW, Shin IS, Hong YJ, Ahn Y, et al. BDNF val66met polymorphism and depressive disorders in patients with acute coronary syndrome. J Affect Disord. 2016; 194: 1-8. doi: 10.1016/j.jad.2016.01.033 PMID: 26795846.