Physical Exercise and Brain-Derived Neurotrophic Factor Concentration in Children and Adolescents: A Systematic Review With Meta-Analysis

in Pediatric Exercise Science
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  • 1 Federal University of Paraná
  • | 2 Federal University of Rio Grande do Sul
  • | 3 University of Porto
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Purpose:To systematically review the literature on the relationship between physical activity and the effect of physical training on brain-derived neurotrophic factor (BDNF) concentrations in children and adolescents. Methods: The searches were conducted in the databases: PubMed, ScienceDirect, Web of Science, Scopus, SPORTDiscus, Latin American and Caribbean Center for Science Information of Health, and SciELO. All original studies that analyzed the relationship between the practice of physical activity and the effect of physical training on plasma and serum BDNF concentrations in children and adolescents were included. The standardized mean difference (SMD), correlation coefficient (r), and 95% confidence interval were calculated. Results: Eleven studies were selected, totaling 1424 children and adolescents. Cross-sectional studies indicated a significant inverse relationship between physical activity and BDNF concentrations in boys (r = −.117 [−.222, −.009]; P = .033), but not in girls (P = .230). Adolescent athletes tend to have lower serum, but higher plasma BDNF concentrations than sedentary ones (SMD = −0.677 [0.188]; P < .001). An increase in serum BDNF was observed after physical training (SMD = 0.437 [0.183]; P = .017), with no effect in the control group (SMD = 0.235 [0.193]; P = .225). Conclusions: Adolescent athletes tend to show lower serum, but higher plasma BDNF concentrations compared with sedentary individuals. Furthermore, physical training seems to increase serum BDNF concentrations in sedentary adolescents to a small extent.

de Menezes-Junior, Jesus, and Leite are with the Department of Physical Education, Federal University of Paraná, Curitiba, Paraná, Brazil. Brand is with the Projeto Esporte Brasil (PROESP-Br), School of Physical Education, Physiotherapy and Dance, Postgraduation Program in Human Movement Sciences, Federal University of Rio Grande do Sul, Porto Alegre, Brazil. Mota is with the Department of Centro de Investigação em Actividade Fìsica, Saúde e Lazer (CIAFEL), University of Porto, Porto, Portugal.

de Menezes Junior (franciscomenezes@ufpr.br) is corresponding author https://orcid.org/0000-0003-4389-1213
  • 1.

    Armstrong N, Mechelen W. Pediatric exercise science and medicine. J Sports Sci Med. 2008;8:349650.

  • 2.

    Li JW, O’Connor H, O’Dwyer N, Orr R. The effect of acute and chronic exercise on cognitive function and academic performance in adolescents: a systematic review. J Sci Med Sport. 2017;20(9):8418. doi:10.1016/j.jsams.2016.11.025

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Esteban-Cornejo I, Reilly J, Ortega FB, Matusik P, Mazur A, Erhardt E, et al. Paediatric obesity and brain functioning: the role of physical activity—A novel and important expert opinion of the European Childhood Obesity Group. Pediatr Obes. 2020;15(9):158. doi:10.1111/ijpo.12649

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Paschen L, Lehmann T, Kehne M, Baumeister J. Effects of acute physical exercise with low and high cognitive demands on executive functions in children: a systematic review. Pediatr Exerc Sci. 2019;31(3):26781. doi:10.1123/pes.2018-0215

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Marinus N, Hansen D, Feys P, Meesen R, Timmermans A, Spildooren J. The impact of different types of exercise training on peripheral blood brain-derived neurotrophic factor concentrations in older adults: a meta-analysis. Sport Med. 2019;49(10):152946. doi:10.1007/s40279-019-01148-z

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Jeon YK, Ha CH. The effect of exercise intensity on brain derived neurotrophic factor and memory in adolescents. Environ Health Prev Med. 2017;22(1):16. doi:10.1186/s12199-017-0643-6

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Griffin ÉW, Mullally S, Foley C, Warmington SA, O’Mara SM, Kelly ÁM. Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol Behav. 2011;104(5):93441. doi:10.1016/j.physbeh.2011.06.005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Walsh JJ, Tschakovsky ME. Exercise and circulating BDNF: mechanisms of release and implications for the design of exercise interventions. Appl Physiol Nutr Metab. 2018;43(11):1095104. doi:10.1139/apnm-2018-0192

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Gejl AK, Enevold C, Bugge A, Andersen MS, Nielsen CH, Andersen LB. Associations between serum and plasma brain-derived neurotrophic factor and influence of storage time and centrifugation strategy. Sci Rep. 2019;9(1):19. doi:10.1038/s41598-019-45976-5

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    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):34753. doi:10.1017/S1461145710000738

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Dinoff A, Herrmann N, Swardfager W, Lanctôt KL. The effect of acute exercise on blood concentrations of brain-derived neurotrophic factor in healthy adults: a meta-analysis. Eur J Neurosci. 2017;46(1):163546. doi:10.1111/ejn.13603

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Dinoff A, Herrmann N, Swardfager W, Liu CS, Sherman C, Chan S, et al. The effect of exercise training on resting concentrations of peripheral brain-derived neurotrophic factor (BDNF): a meta-analysis. PLoS One. 2016;11(9):121. doi:10.1371/journal.pone.0163037

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Huang T, Gejl AK, Tarp J, Andersen LB, Peijs L, Bugge A. Cross-sectional associations of objectively measured physical activity with brain-derived neurotrophic factor in adolescents. Physiol Behav. 2017;171:8791. PubMed ID: 28027935 doi:10.1016/j.physbeh.2016.12.026

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Mora-Gonzalez J, Migueles JH, Esteban-Cornejo I, Cadenas-Sanchez C, Pastor-Villaescusa B, Molina-García P, et al. Sedentarism, physical activity, steps, and neurotrophic factors in obese children. Med Sci Sports Exerc. 2019;51(11):232533. doi:10.1249/MSS.0000000000002064

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Beltran-Valls MR, Adelantado-Renau M, Moliner-Urdiales D. Association between objectively measured physical activity and plasma BDNF in adolescents: DADOS Study. J Mol Neurosci. 2018;65(4):46771. doi:10.1007/s12031-018-1122-2

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Arvidsson D, Johannesson E, Andersen LB, Karlsson M, Wollmer P, Thorsson O, et al. A longitudinal analysis of the relationships of physical activity and body fat with nerve growth factor and brain-derived neural factor in children. J Phys Act Heal. 2018;15(8):6205. doi:10.1123/jpah.2017-0483

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Lee TMC, Wong ML, Lau BW-M, Lee JC-D, Yau S-Y, So K-F. Aerobic exercise interacts with neurotrophic factors to predict cognitive functioning in adolescents. Psychoneuroendocrinology. 2014;37(1):21424. doi:10.1016/j.psyneuen.2011.05.006

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Yang L, Cao C, Kantor ED, Nguyen LH, Zheng X, Park Y, et al. Trends in sedentary behavior among the US population, 2001–2016. JAMA. 2019;321(16):158797. doi:10.1001/jama.2019.3636

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097. PubMed ID: 19621072 doi:10.1371/journal.pmed.1000097

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Higgins JP, Green S. Cochrane Handbook for Systematic Reviews of Interventions. Cochrane Book Series. UK: John Wiley & Sons, Ltd; 2008. doi:10.1002/9780470712184

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    WHO. Global Recommendations on Physical Activity for Health. Geneva: WHO; 2010.

  • 22.

    Downs SH, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Heal. 1998;52(6):37784. doi:10.1136/jech.52.6.377

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Tremblay MS, LeBlanc AG, Kho ME, Saunders TJ, Larouche R, Colley RC, et al. Systematic review of sedentary behaviour and health indicators in school-aged children and youth. Int J Behav Nutr Phys Act. 2011;8(1):98. doi:10.1186/1479-5868-8-98

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):153958. doi:10.1002/sim.1186

  • 25.

    Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):62934. doi:10.1136/bmj.315.7109.629

  • 26.

    Kim Y II. The impact of exercise training on basal bdnf in athletic adolescents. J Phys Ther Sci. 2016;28(11):30669. doi:10.1589/jpts.28.3066

  • 27.

    Pareja-Galeano H, Brioche T, Sanchis-Gomar F, Montal A, Jovani C, Martinez-Costa C, et al. Impact of exercise training on neuroplasticity-related growth factors in adolescents. J Musculoskelet Neuronal Interact. 2013;13(3):36871.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Goldfield GS, Kenny GP, Prud’homme D, Holcik M, Alberga AS, Fahnestock M, et al. Effects of aerobic training, resistance training, or both on brain-derived neurotrophic factor in adolescents with obesity: the hearty randomized controlled trial. Physiol Behav. 2018;191:13845. doi:10.1016/j.physbeh.2018.04.026

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Cho SY, So WY, Roh HT. The effects of taekwondo training on peripheral neuroplasticity-related growth factors, cerebral blood flow velocity, and cognitive functions in healthy children: a randomized controlled trial. Int J Environ Res Public Health. 2017;14(5):110. doi:10.3390/ijerph14050454

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Jeon YK, Ha CH. Expression of brain-derived neurotrophic factor, IGF-1 and cortisol elicited by regular aerobic exercise in adolescents. J Phys Ther Sci. 2015;27(3):73741. doi:10.1589/jpts.27.737

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Fujimura H, Altar C, 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(04):728734. doi:10.1055/s-0037-1613072

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Gibbs RB. Treatment with estrogen and progesterone affects relative levels of brain-derived neurotrophic factor mRNA and protein in different regions of the adult rat brain. Brain Res. 1999;844(1–2):207. doi:10.1016/s0006-8993(99)01880-6

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Gimenez M, Mohan-Kumar T, Humbert JC, De Talance N, Buisine J. Leukocyte, lymphocyte and platelet response to dynamic exercise. Eur J Appl Physiol Occup Physiol. 1986;55(5):465470. PubMed ID: 3769902 doi:10.1007/BF00421638

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci. 2001;24:677736. doi:10.1146/annurev.neuro.24.1.677

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Iughetti L, Casarosa E, Predieri B, Patianna V, Luisi S. Plasma brain-derived neurotrophic factor concentrations in children and adolescents. Neuropeptides. 2011;45(3):20511. doi:10.1016/j.npep.2011.02.002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Scharfman HE, Mercurio TC, Goodman JH, Wilson MA, MacLusky NJ. Hippocampal excitability increases during the estrous cycle in the rat: a potential role for brain-derived neurotrophic factor. J Neurosci. 2003;23(37):1164152. doi:10.1523/JNEUROSCI.23-37-11641.2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Scharfman HE, MacLusky NJ. EstrogenGrowth factor interactions and their contributions to neurological disorders. Headache J Head Face Pain. 2008;48:S7789. doi:10.1111/j.1526-4610.2008.01200.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Begliuomini S, Casarosa E, Pluchino N, Lenzi E, Centofanti M, Freschi L, et al. Influence of endogenous and exogenous sex hormones on plasma brain-derived neurotrophic factor. Hum Reprod. 2007;22(4):9951002. doi:10.1093/humrep/del479

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Motamedi S, Karimi I, Jafari F. The interrelationship of metabolic syndrome and neurodegenerative diseases with focus on brain-derived neurotrophic factor (BDNF): Kill two birds with one stone. Metab Brain Dis. 2017;32(3):65165. doi:10.1007/s11011-017-9997-0

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    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):4318. PubMed ID: 17151862 doi:10.1007/s00125-006-0537-4

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Walsh JJ, Myette-Côté É, Little JP. The effect of exogenous ketone monoester ingestion on plasma BDNF during an oral glucose tolerance test. Front Physiol. 2020;11:1094. PubMed ID: 33013465 doi:10.3389/fphys.2020.01094

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Roth CL, Elfers C, Gebhardt U, Müller HL, Reinehr T. Brain-derived neurotrophic factor and its relation to leptin in obese children before and after weight loss. Metabolism. 2013;62(2):226234. PubMed ID: 23040414 doi:10.1016/j.metabol.2012.08.001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Walsh JJ, Bentley RF, Gurd BJ, Tschakovsky ME. Short-Duration maximal and long-duration submaximal effort forearm exercise achieve elevations in serum brain-derived neurotrophic factor. Front Physiol. 2017;8:746. doi:10.3389/fphys.2017.00746

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Pan W, Banks WA, Fasold MB, Bluth J, Kastin AJ. Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology. 1998;37(12):155361. doi:10.1016/S0028-3908(98)00141-5

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    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):301722. doi:10.1073/pnas.1015950108

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    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. Sport Med. 2010;40(9):765801. doi:10.2165/11534530-000000000-00000

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47.

    Reycraft JT, Islam H, Townsend LK, Hayward GC, Hazell TJ, MacPherson REK. Exercise intensity and recovery on circulating brain-derived neurotrophic factor. Med Sci Sports Exerc. 2019;52(5):12101217. doi:10.1249/MSS.0000000000002242

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 48.

    Brooks GA. Lactate as a fulcrum of metabolism. Redox Biol. 2020;35(January):101454. doi:10.1016/j.redox.2020.101454

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