A meta-analytic review of the effects of exercise on brain-derived neurotrophic factor

Journal of Psychiatric Research

Volumn 60, Issue , 2015, Pages 56-64

  Szuhany, Kristin L ^a   Bugatti, Matteo ^a   Otto, Michael W ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

BDNF; Brain derived neurotrophic factor; Exercise; Meta analysis; Physical activity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

COGNITION; EXERCISE; EXERCISE INTENSITY; HUMAN; LEARNING; MAJOR DEPRESSION; PANIC; PHYSICAL ACTIVITY; RESISTANCE TRAINING; REVIEW; ADULT; AGE; BLOOD; FEMALE; MALE; META ANALYSIS; MOTOR ACTIVITY; PHYSIOLOGY; PSYCHOLOGY; SEX DIFFERENCE; TIME FACTOR;

ADULT; AGE FACTORS; BRAIN-DERIVED NEUROTROPHIC FACTOR; EXERCISE; FEMALE; HUMANS; MALE; MOTOR ACTIVITY; SEX FACTORS; TIME FACTORS;

EID: 84919389649     PISSN: 00223956     EISSN: 18791379     Source Type: Journal    
DOI: 10.1016/j.jpsychires.2014.10.003     Document Type: Review

References (85)

1. Ahlskog J.E. Does vigorous exercise have a neuroprotective effect in Parkinson disease?. Neurology 2011, 77:288-294.
2. Alford L. What men should know about the impact of physical activity on their health. Int J Clin Pract 2010, 64:1731-1734.
3. Altar C.A. Neurotrophins and depression. Trends Pharmacol Sci 1999, 20:59-62.
4. 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, 59:1-4.
5. Araya A.V., 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, 45:541-544.
6. Asmundson G.J., Fetzner M.G., Deboer L.B., Powers M.B., Otto M.W., Smits J.A. Let's get physical: a contemporary review of the anxiolytic effects of exercise for anxiety and its disorders. Depress Anxiety 2013, 30:362-373.
7. Baker L.D., Frank L.L., Foster-Schubert K., Green P.S., Wilkinson C.W., McTiernan A., et al. Effects of aerobic exercise on mild cognitive impairment: a controlled trial. Archiv Neurol 2010, 67:71-79
8. Bansi J., Bloch W., Gamper U., Kesselring J. Training in MS: influence of two different endurance training protocols (aquatic versus overland) on cytokine and neurotrophin concentrations during three week randomized controlled trial. Mult Scler (Houndmills, Basingstoke, England) 2013, 19:613-621
9. Blair S.N., Haskell W.L., Ho P., Paffenbarger R.S., Vranizan K.M., Farquhar J.W., et al. Assessment of habitual physical activity by a seven-day recall in a community survey and controlled experiments. Am J Epidemiol 1985, 122:794-804.
10. Bornstein M., Hedges L.V., Higgins J., Rothstein H. Comprehensive meta-analysis, version 2 2005, Biostat Inc., Englewood, NJ.
11. Bos I., De Boever P., Vanparijs J., Pattyn N., Panis L.I., Meeusen R. Subclinical effects of aerobic training in urban environment. Med Sci Sports Exerc 2013, 45:439-447
12. Bos I., Jacobs L., Nawrot T.S., de Geus B., Torfs R., Int Panis L., et al. No exercise-induced increase in serum BDNF after cycling near a major traffic road. Neurosci Lett 2011, 500:129-132
13. Brunelli A., Dimauro I., Sgro P., Emerenziani G.P., Magi F., Baldari C., et al. Acute exercise modulates BDNF and pro-BDNF protein content in immune cells. Med Sci Sports Exerc 2012, 44:1871-1880
14. Brunoni A.R., Lopes M., Fregni F. Asystematic review and meta-analysis of clinical studies on major depression and BDNF levels: implications for the role of neuroplasticity in depression. Int J neuropsychopharmacology/Off Sci J Coll Int Neuropsychopharmacol (CINP) 2008, 11:1169-1180.
15. Castellano V., White L.J. Serum brain-derived neurotrophic factor response to aerobic exercise in multiple sclerosis. JNeurol Sci 2008, 269:85-91
16. Cho H.C., Kim J., Kim S., Son Y.H., Lee N., Jung S.H. The concentrations of serum, plasma and platelet BDNF are all increased by treadmill VO(2)max performance in healthy college men. Neurosci Lett 2012, 519:78-83
17. Christie B.R., Eadie B.D., Kannangara T.S., Robillard J.M., Shin J., Titterness A.K. Exercising our brains: how physical activity impacts synaptic plasticity in the dentate gyrus. Neuromolecular Med 2008, 10:47-58.
18. Cohen J.A. power primer. Psychol Bull 1992, 112:155.
19. Correia P.R., Pansani A., Machado F., Andrade M., Silva A.C., Scorza F.A., et al. Acute strength exercise and the involvement of small or large muscle mass on plasma brain-derived neurotrophic factor levels. Clinics (Sao Paulo, Brazil) 2010, 65:1123-1126
20. Corripio R., Gonzalez-Clemente J.M., Jacobo P.S., Silvia N., Lluis G., Joan V., et al. Plasma brain-derived neurotrophic factor in prepubertal obese children: results from a 2-year lifestyle intervention programme. Clin Endocrinol 2012, 77:715-720
21. Cotman C.W., Berchtold N.C., Christie L.-A. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 2007, 30:464-472.
22. Craig C.L., Marshall A.L., Sjostrom M., Bauman A.E., Booth M.L., Ainsworth B.E., et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 2003, 195:1381-1395.
23. Duman R.S., Monteggia L.M. Aneurotrophic model for stress-related mood disorders. Biol Psychiatry 2006, 59:1116-1127.
24. Egan M.F., Kojima M., Callicott J.H., Goldberg T.E., Kolachana B.S., Bertolino A., et al. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 2003, 112:257-269.
25. Erickson K.I., Miller D.L., Roecklein K.A. The aging hippocampus: interactions between exercise, depression, and BDNF. Neurosci: a Rev J Bringing Neurobiol Neurol Psychiatry 2012, 18:82-97.
26. Erickson K.I., Prakash R.S., Voss M.W., Chaddock L., Hu L., Morris K.S., et al. Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus 2009, 19:1030-1039.
27. Erickson K.I., Voss M.W., Prakash R.S., Basak C., Szabo A., Chaddock L., et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A 2011, 108:3017-3022
28. Field A.P. Meta-analysis of correlation coefficients: a Monte Carlo comparison of fixed- and random-effects methods. Psychol Method 2001, 6:161-180.
29. Forbes D., Thiessen E.J., Blake C.M., Forbes S.C., Forbes S. Exercise programs for people with dementia. Cochrane Database Syst Rev 2013, 12:CD006489.
30. Follmann D., Elliott P., Suh I.L., Cutler J. Variance imputation for overviews of clinical trials with continuous response. J Clin Epidemiol 1992, 45(7):769-773.
31. Garber C.E., Blissmer B., Deschenes M.R., Franklin B.A., Lamonte M.J., Lee I.-M., et al. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc 2011, 43:1334-1359. 10.249/MSS.0b013e318213fefb.
32. 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, 110:285-293
33. Goekint M., Heyman E., Roelands B., Njemini R., Bautmans I., Mets T., et al. No influence of noradrenaline manipulation on acute exercise-induced increase of brain-derived neurotrophic factor. Med Sci Sports Exerc 2008, 40:1990-1996
34. Gorski J.A., Zeiler S.R., Tamowski S., Jones K.R. Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites. JNeurosci 2003, 23:6856-6865.
35. Grassi-Oliveira R., Stein L.M., Lopes R.P., Teixeira A.L., Bauer M.E. Low plasma brain-derived neurotrophic factor and childhood physical neglect are associated with verbal memory impairment in major depression-a preliminary report. Biol Psychiatry 2008, 64:281-285.
36. Griffin E.W., Mullally S., Foley C., Warmington S.A., O'Mara S.M., Kelly A.M. Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol Behav 2011, 104:934-941
37. Gustafsson G., Lira C.M., Johansson J., Wisen A., Wohlfart B., Ekman R., 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
38. Hedges L.V., Olkin I. Statistical methods for meta-analysis 1985, Academic Press, San Diego, CA.
39. Heyman E., Gamelin F.X., Goekint M., Piscitelli F., Roelands B., Leclair E., et al. Intense exercise increases circulating endocannabinoid and BDNF levels in humans-possible implications for reward and depression. Psychoneuroendocrinology 2012, 37:844-851.
40. Hopkins M.E., Nitecki R., Bucci D.J. Physical exercise during adolescence versus adulthood: differential effects on object recognition memory and brain-derived neurotrophic factor levels. Neurosci 2011, 194:84-94.
41. Huang T., Larsen K.T., Ried-Larsen M., Moller N.C., Andersen L.B. The effects of physical activity and exercise on brain-derived neurotrophic factor in healthy humans: a review. Scand J Med Sci Sports 2014, 24:1-10.
42. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 1999, 98:739-755.
43. Hunter J.E., Schmidt F.L. Methods of meta-analysis: correcting error and bias in research findings 2004, Sage.
44. Intlekofer K.A., Berchtold N.C., Malvaez M., Carlos A.J., McQuown S.C., Cunningham M.J., et al. Exercise and sodium butyrate transform a subthreshold learning event into long-term memory via a brain-derived neurotrophic factor-dependent mechanism. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 2013, 38:2027-2034.
45. Josefsson T., Lindwall M., Archer T. Physical exercise intervention in depressive disorders: meta-analysis and systematic review. Scand J Med Sci Sports 2014, 24:259-272.
46. Karege F., Schwald M., Cisse M. Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets. Neurosci Lett 2002, 328:261-264.
47. Komulainen P., Pedersen M., Hanninen T., Bruunsgaard H., Lakka T.A., Kivipelto M., 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.
48. Korol D.L., Gold P.E., Scavuzzo C.J. Use it and boost it with physical and mental activity. Hippocampus 2013, 23:1125-1135.
49. Krabbe K.S., Nielsen A.R., Krogh-Madsen R., Plomgaard P., Rasmussen P., Erikstrup C., et al. Brain-derived neurotrophic factor (BDNF) and type 2 diabetes. Diabetologia 2007, 50:431-438.
50. 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 Neuropsychopharmacol 2010, 13:595-602
51. Lipsey M.W., Wilson D.B. Practical meta-analysis 2000, Sage Publications, Thousand Oaks, CA.
52. Lu B., Pang P.T., Woo N.H. The yin and yang of neurotrophin action. Nat Rev Neurosci 2005, 6:603-614.
53. 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.
54. Oertel-Knochel V., Mehler P., Thiel C., Steinbrecher K., Malchow B., Tesky V., et al. Effects of aerobic exercise on cognitive performance and individual psychopathology in depressive and schizophrenia patients. Eur Archiv Psychiatry Clin Neurosci 2014, 264(7):589-604.
55. Phillips C., Baktir M.A., Srivatsan M., Salehi A. Neuroprotective effects of physical activity on the brain: a closer look at trophic factor signaling. Front Cell Neurosci 2014, 8:170.
56. Piccinni A., Marazziti D., Catena M., Domenici L., Del Debbio A., Bianchi C., et al. Plasma and serum brain-derived neurotrophic factor (BDNF) in depressed patients during 1 year of antidepressant treatments. JAffect Disord 2008, 105:279-283.
57. Rasmussen P., Brassard P., Adser H., Pedersen M.V., Leick L., Hart E., et al. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp Physiol 2009, 94:1062-1069
58. Rethorst C.D., Trivedi M.H. Evidence-based recommendations for the prescription of exercise for major depressive disorder. JPsychiatric Pract 2013, 19:204-212.
59. Rex C.S., Lauterborn J.C., Lin C.-Y., Kramár E.A., Rogers G.A., Gall C.M., et al. Restoration of long-term potentiation in middle-aged hippocampus after induction of brain-derived neurotrophic factor. JNeurophysiol 2006, 96:677-685.
60. Roig M., Nordbrandt S., Geertsen S.S., Nielsen J.B. The effects of cardiovascular exercise on human memory: a review with meta-analysis. Neurosci Biobehav Rev 2013, 37:1645-1666.
61. Rojas Vega S.R., Kleinert J., Sulprizio M., Hollmann W., Bloch W., Struder H.K. Responses of serum neurotrophic factors to exercise in pregnant and postpartum women. Psychoneuroendocrinology 2011, 36:220-227
62. Rosenthal R. Meta-analytic procedures for social research 1991, Sage.
63. Rosenthal R., Rubin D.B. [Selection models and the file drawer problem]: comment: assumptions and procedures in the file drawer problem. Stat Sci 1988, 3:120-125.
64. Ruscheweyh R., Willemer C., Kruger K., Duning T., Warnecke T., Sommer J., et al. Physical activity and memory functions: an interventional study. Neurobiol Aging 2011, 32:1304-1319
65. Schiffer T., Schulte S., Hollmann W., Bloch W., Struder H.K. Effects of strength and endurance training on brain-derived neurotrophic factor and insulin-like growth factor 1 in humans. Horm Metab Res 2009, 41:250-254
66. Schmidt H.D., Duman R.S. Peripheral BDNF produces antidepressant-like effects in cellular and behavioral models. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 2010, 35:2378-2391.
67. Schmidt-Kassow M., Schadle S., Otterbein S., Thiel C., Doehring A., Lotsch J., et al. Kinetics of serum brain-derived neurotrophic factor following low-intensity versus high-intensity exercise in men and women. Neuroreport 2012, 23:889-893
68. Schulz K.H., Gold S.M., Witte J., Bartsch K., Lang U.E., Hellweg R., et al. Impact of aerobic training on immune-endocrine parameters, neurotrophic factors, quality of life and coordinative function in multiple sclerosis. JNeurological Sci 2004, 225:11-18
69. 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:R372-R377
70. 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.
71. Siette J., Westbrook R.F., Cotman C., Sidhu K., Zhu W., Sachdev P., et al. Age-specific effects of voluntary exercise on memory and the older brain. Biol Psychiatry 2013, 73:435-442.
72. Smith P.J., Blumenthal J.A., Hoffman B.M., Cooper H., Strauman T.A., Welsh-Bohmer K., et al. Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosom Med 2010, 72:239-252.
73. Stathopoulou G., Powers M.B., Berry A.C., Smits J.A.J., Otto M.W. Exercise interventions for mental health: a quantitative and qualitative review. Clin Psychol Sci Pract 2006, 13:179-193.
74. Strohle A., Stoy M., Graetz B., Scheel M., Wittmann A., Gallinat J., et al. Acute exercise ameliorates reduced brain-derived neurotrophic factor in patients with panic disorder. Psychoneuroendocrinology 2010, 35:364-368
75. Swift D.L., Johannsen N.M., Myers V.H., Earnest C.P., Smits J.A., Blair S.N., et al. The effect of exercise training modality on serum brain derived neurotrophic factor levels in individuals with type 2 diabetes. PloS One 2012, 7:e42785
76. Tang S.W., Chu E., Hui T., Helmeste D., Law C. Influence of exercise on serum brain-derived neurotrophic factor concentrations in healthy human subjects. Neurosci Lett 2008, 431:62-65
77. Toups M.S., Greer T.L., Kurian B.T., Grannemann B.D., Carmody T.J., Huebinger R., et al. Effects of serum brain derived neurotrophic factor on exercise augmentation treatment of depression. JPsychiatric Res 2011, 45:1301-1306
78. van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. JNeurosci: Off J Soc Neurosci 2005, 25:8680-8685.
79. Vaynman S., Ying Z., Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 2004, 20:2580-2590.
80. Whiteman A.S., Young D.E., He X., Chen T.C., Wagenaar R.C., Stern C.E., et al. Interaction between serum BDNF and aerobic fitness predicts recognition memory in healthy young adults. Behav Brain Res 2014, 259:302-312.
81. Yang J.L., Lin Y.T., Chuang P.C., Bohr V.A., Mattson M.P. BDNF and exercise enhance neuronal DNA repair by stimulating CREB-mediated production of apurinic/apyrimidinic endonuclease 1. Neuromolecular Med 2014, 16:161-174.
82. 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
83. Zagaar M., Dao A., Alhaider I., Alkadhi K. Regular treadmill exercise prevents sleep deprivation-induced disruption of synaptic plasticity and associated signaling cascade in the dentate gyrus. Mol Cell Neurosci 2013, 56:375-383.
84. Zoladz J.A., Pilc A. The effect of physical activity on the brain derived neurotrophic factor: from animal to human studies. JPhysiol Pharmacol: Off J Pol physiol Soc 2010, 61:533-541.
85. Zoladz J.A., Pilc A., Majerczak J., Grandys M., Zapart-Bukowska J., Duda K. Endurance training increases plasma brain-derived neurotrophic factor concentration in young healthy men. JPhysiol Pharmacol: Off J Pol Physiol Soc 2008, 59(Suppl.7):119-132