Neurobiological effects of exercise on major depressive disorder: A systematic review

Neuroscience and Biobehavioral Reviews

Volumn 61, Issue , 2016, Pages 1-11

  Schuch, Felipe Barreto ^a,b   Deslandes, Andrea Camaz ^c   Stubbs, Brendon ^d,e   Gosmann, Natan Pereira ^b   Silva, Cristiano Tschiedel Belem da ^a,b   Fleck, Marcelo Pio de Almeida ^a,b  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

^c STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e SOUTH LONDON AND MAUDSLEY NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Depression; Exercise; Hormones; Immobilization; Inflammation; Neuronal activity; Neuroplasticity; Neurotrophines; Oxidative stress chitosan; PVC cable; Termite control

Indexed keywords

ATRIAL NATRIURETIC FACTOR; BIOLOGICAL MARKER; BRAIN NATRIURETIC PEPTIDE; COPEPTIN; GROWTH HORMONE; INTERLEUKIN 1BETA; PROLACTIN; THIOBARBITURIC ACID REACTIVE SUBSTANCE; ANTIDEPRESSANT AGENT;

BRAIN SIZE; CORTICAL THICKNESS (BRAIN); DISEASE ASSOCIATION; ELECTROENCEPHALOGRAM; EXERCISE; HIPPOCAMPUS; HORMONE BLOOD LEVEL; HUMAN; MAJOR DEPRESSION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROENDOCRINOLOGY; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SYSTEMATIC REVIEW; THERAPY EFFECT; TREATMENT RESPONSE; ANIMAL; BRAIN; DEPRESSION; DEPRESSIVE DISORDER, MAJOR; DRUG EFFECTS; PATHOPHYSIOLOGY; PHYSIOLOGY; TREATMENT OUTCOME;

ANIMALS; ANTIDEPRESSIVE AGENTS; BRAIN; DEPRESSION; DEPRESSIVE DISORDER, MAJOR; EXERCISE; HUMANS; TREATMENT OUTCOME;

EID: 84949665243     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2015.11.012     Document Type: Review

References (93)

1. Belmaker R.H., Agam G. Major depressive disorder. N Engl J Med 2008, 358:55-68.
2. Bloomer R.J., Goldfarb A.H. Anaerobic exercise and oxidative stress: a review. Can J Appl Physiol 2004, 29:245-263.
3. Bloomer R.J., Goldfarb A.H., Wideman L., McKenzie M.J., Consitt L.A. Effects of acute aerobic and anaerobic exercise on blood markers of oxidative stress. J Strength Cond Res 2005, 19:276-285.
4. Blumenthal J.A., Babyak M.A., Doraiswamy P.M., Watkins L., Hoffman B.M., Barbour K.A., Herman S., Craighead W.E., Brosse A.L., Waugh R., Hinderliter A., Sherwood A. Exercise and pharmacotherapy in the treatment of major depressive disorder. Psychosom Med 2007, 69:587-596.
5. Blumenthal J.A., Babyak M.A., Moore K.A., Craighead W.E., Herman S., Khatri P., Waugh R., Napolitano M.A., Forman L.M., Appelbaum M., Doraiswamy P.M., Krishnan K.R. Effects of exercise training on older patients with major depression. Arch Intern Med 1999, 159:2349-2356.
6. Blumenthal J.A., Babyak M.A., O'Connor C., et al. Effects of exercise training on depressive symptoms in patients with chronic heart failure: the hf-action randomized trial. JAMA 2012, 308:465-474.
7. Boettger S., Müller H.-J., Oswald K., Puta C., Donath L., Gabriel H.H.W., Bär K.-J. Inflammatory changes upon a single maximal exercise test in depressed patients and healthy controls. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:475-478.
8. Brown-Borg H.M., Rakoczy S.G., Romanick M.A., Kennedy M.A. Effects of growth hormone and insulin-like growth factor-1 on hepatocyte antioxidative enzymes. Exp Biol Med 2002, 227:94-104.
9. 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.
10. Cassilhas R.C., Lee K.S., Fernandes J., Oliveira M.G., Tufik S., Meeusen R., de Mello M.T. Spatial memory is improved by aerobic and resistance exercise through divergent molecular mechanisms. Neuroscience 2012, 202:309-317.
11. Cohen J. Statistical Power Analysis for the Behavioral Sciences 1988, Academic Press, San Diego, CA.
12. Cooney G.M., Dwan K., Greig C.A., Lawlor D.A., Rimer J., Waugh F.R., McMurdo M., Mead G.E. Exercise for depression. Cochrane Database Syst Rev 2013, 9:CD004366.
13. Craft L.L., Landers D.M. The effects of exercise on clinical depression and depression resulting from mental illness: a meta-regression analysis. J Sport Exerc Psychol 1998, 20:339-357.
14. Daley A. Exercise and depression: a review of reviews. J Clin Psychol Med Settings 2008, 15:140-147.
15. Danielsson L., Noras A.M., Waern M., Carlsson J. Exercise in the treatment of major depression: a systematic review grading the quality of evidence. Physiother Theory Pract 2013, 29:573-585.
16. Deslandes A.C., Moraes H., Alves H., Pompeu F.A., Silveira H., Mouta R., Arcoverde C., Ribeiro P., Cagy M., Piedade R.A., Laks J., Coutinho E.S. Effect of aerobic training on EEG alpha asymmetry and depressive symptoms in the elderly: a 1-year follow-up study. Braz J Med Biol Res 2010, 43:585-592.
17. Dowlati Y., Herrmann N., Swardfager W., Liu H., Sham L., Reim E.K., Lanctot K.L. A meta-analysis of cytokines in major depression. Biol Psychiatry 2010, 67:446-457.
18. Dunn A.L., Trivedi M.H., Kampert J.B., Clark C.G., Chambliss H.O. Exercise treatment for depression: efficacy and dose response. Am J Prev Med 2005, 28:1-8.
19. Eyre H., Baune B.T. Neuroimmunological effects of physical exercise in depression. Brain Behavior Immun 2012, 26:251-266.
20. Eyre H., Baune B.T. Neuroplastic changes in depression: a role for the immune system. Psychoneuroendocrinology 2012, 37:1397-1416.
21. Eyre H.A., Papps E., Baune B.T. Treating depression and depression-like behavior with physical activity: an immune perspective. Front Psychiatry 2013, 4.
22. Ferrari A.J., Charlson F.J., Norman R.E., Patten S.B., Freedman G., Murray C.J., Vos T., Whiteford H.A. Burden of depressive disorders by country, sex, age, and year: findings from the global burden of disease study 2010. PLoS Med 2013, 10:e1001547.
23. Filser J.G., Spira J., Fischer M., Gattaz W.F., Muller W.E. The evaluation of 4-hydroxy-3-methoxyphenylglycol sulfate as a possible marker of central norepinephrine turnover. Studies in healthy volunteers and depressed patients. J Psychiatr Res 1988, 22:171-181.
24. Foley L.S., Prapavessis H., Osuch E.A., De Pace J.A., Murphy B.A., Podolinsky N.J. An examination of potential mechanisms for exercise as a treatment for depression: a pilot study. Ment Health Phys Activity 2008, 1:69-73.
25. Fuqua J.S., Rogol A.D. Neuroendocrine alterations in the exercising human: implications for energy homeostasis. Metabolism 2013, 62:911-921.
26. Furtado M., Katzman M.A. Examining the role of neuroinflammation in major depression. Psychiatry Res. 2015, 229(September (1-2)):27-36. 10.1016/j.psychres.2015.06.009.
27. Goekint M., Roelands B., Heyman E., Njemini R., Meeusen R. Influence of citalopram and environmental temperature on exercise-induced changes in BDNF. Neurosci Lett 2011, 494:150-154.
28. Gustafsson G., Lira C.M., Johansson J., Wisen A., Wohlfart B., Ekman R., Westrin A. The acute response of plasma brain-derived neurotrophic factor as a result of exercise in major depressive disorder. Psychiatry Res 2009, 169:244-248.
29. Hallberg L., Janelidze S., Engstrom G., Wisén A.G.M., Westrin Å., Brundin L. Exercise-induced release of cytokines in patients with major depressive disorder. J Affect Disord 2010, 126:262-267.
30. Hamilton J.P., Etkin A., Furman D.J., Lemus M.G., Johnson R.F., Gotlib I.H. Functional neuroimaging of major depressive disorder: a meta-analysis and new integration of base line activation and neural response data. Am J Psychiatry 2012, 169:693-703.
31. Hedges L.V., Olkin I. Statistical Method for Meta-analysis 2014, Academic Press.
32. Hennings A., Schwarz M.J., Riemer S., Stapf T.M., Selberdinger V.B., Rief W. Exercise affects symptom severity but not biological measures in depression and somatization-results on IL-6, neopterin, tryptophan, kynurenine and 5-HIAA. Psychiatry Res 2013, 210:925-933.
33. 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.
34. 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.
35. Katan M., Morgenthaler N., Widmer I., Puder J.J., Konig C., Muller B., Christ-Crain M. Copeptin, a stable peptide derived from the vasopressin precursor, correlates with the individual stress level. Neuroendocrinol Lett 2008, 29:341-346.
36. Kiive E., Maaroos J., Shlik J., Tõru I., Harro J. Growth hormone, cortisol and prolactin responses to physical exercise: higher prolactin response in depressed patients. Prog Neuropsychopharmacol Biol Psychiatry 2004, 28:1007-1013.
37. Knaepen K., Goekint M., Heyman E.M., Meeusen R. Neuroplasticity-exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects. Sports Med 2010, 40:765-801. 710.2165/11534530-000000000-000000000.
38. Kremen W.S., O'Brien R.C., Panizzon M.S., Prom-Wormley E., Eaves L.J., Eisen S.A., Eyler L.T., Hauger R.L., Fennema-Notestine C., Fischl B., Grant M.D., Hellhammer D.H., Jak A.J., Jacobson K.C., Jernigan T.L., Lupien S.J., Lyons M.J., Mendoza S.P., Neale M.C., Seidman L.J., Thermenos H.W., Tsuang M.T., Dale A.M., Franz C.E. Salivary cortisol and prefrontal cortical thickness in middle-aged men: a twin study. Neuroimage 2010, 53:1093-1102.
39. Krogh J., Benros M.E., Jorgensen M.B., Vesterager L., Elfving B., Nordentoft M. The association between depressive symptoms, cognitive function, and inflammation in major depression. Brain Behav Immun 2014, 35:70-76.
40. Krogh J., Gotze J.P., Jorgensen M.B., Kristensen L.O., Kistorp C., Nordentoft M. Copeptin during rest and exercise in major depression. J Affect Disord 2013, 151:284-290.
41. Krogh J., Nordentoft M., Mohammad-Nezhad M., Westrin Å. Growth hormone, prolactin and cortisol response to exercise in patients with depression. J Affect Disord 2010, 125:189-197.
42. Krogh J., Nordentoft M., Sterne J.A., Lawlor D.A. The effect of exercise in clinically depressed adults: systematic review and meta-analysis of randomized controlled trials. J Clin Psychiatry 2011, 72:529-538.
43. Krogh J., Rostrup E., Thomsen C., Elfving B., Videbech P., Nordentoft M. The effect of exercise on hippocampal volume and neurotrophines in patients with major depression-a randomized clinical trial. J Affect Disord 2014, 165:24-30.
44. Krogh J., Saltin B., Gluud C., Nordentoft M. The DEMO trial: a randomized, parallel-group, observer-blinded clinical trial of strength versus aerobic versus relaxation training for patients with mild to moderate depression. J Clin Psychiatry 2009, 70:790-800.
45. Krogh J., Strohle A., Westrin T., Klausen T., Jorgensen M.B., Nordentoft M. N-terminal pro-atrial natriuretic peptide response to acute exercise in depressed patients and healthy controls. Psychoneuroendocrinology 2011, 36:656-663.
46. Krogh J., Videbech P., Thomsen C., Gluud C., Nordentoft M. DEMO-II trial. Aerobic exercise versus stretching exercise in patients with major depression-a randomised clinical trial. PLoS One 2012, 7:e48316.
47. Leal-Cerro A., Gippini A., Amaya M.J., Lage M., Mato J.A., Dieguez C., Casanueva F.F. Mechanisms underlying the neuroendocrine response to physical exercise. J Endocrinol Invest 2003, 26:879-885.
48. Lechin F., van der Dijs B., Orozco B., Lechin M.E., Báez S., Lechin A.E., Rada I., Acosta E., Arocha L., Jiménez V., León G., García Z. Plasma neurotransmitters, blood pressure, and heart rate during supine-resting, orthostasis, and moderate exercise conditions in major depressed patients. Biological Psychiatry 1995, 38:166-173.
49. Leonard B.E. Impact of inflammation on neurotransmitter changes in major depression: an insight into the action of antidepressants. Prog Neuropsychopharmacol Biol Psychiatry 2014, 48:261-267.
50. Lichtman J.H., Froelicher E.S., Blumenthal J.A., Carney R.M., Doering L.V., Frasure-Smith N., Freedland K.E., Jaffe A.S., Leifheit-Limson E.C., Sheps D.S., Vaccarino V., Wulsin L. Depression as a risk factor for poor prognosis among patients with acute coronary syndrome: systematic review and recommendations: a scientific statement from the American Heart Association. Circulation 2014, 129:1350-1369.
51. Lopresti A.L., Maker G.L., Hood S.D., Drummond P.D. A review of peripheral biomarkers in major depression: the potential of inflammatory and oxidative stress biomarkers. Prog Neuropsychopharmacol Biol Psychiatry 2014, 48:102-111.
52. Matta Mello Portugal E., Cevada T., Sobral Monteiro-Junior R., Teixeira Guimarães T., da Cruz Rubini E., Lattari E., Blois C., Camaz Deslandes A. Neuroscience of exercise: from neurobiology mechanisms to mental health. Neuropsychobiology 2013, 68:1-14.
53. Medina J.L., Jacquart J., Smits J.A.J. Optimizing the exercise prescription for depression: the search for biomarkers of response. Curr Opin Psychol 2015, 4:43-47.
54. Meeusen R. Exercise and the brain: insight in new therapeutic modalities. Ann Transplant 2005, 10:49-51.
55. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry 2009, 65:732-741.
56. Moher D., Liberati A., Tetzlaff J., Altman D.G. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009, 6:e1000097.
57. Morales-Alamo D., Calbet J.A. Free radicals and sprint exercise in humans. Free Radic Res 2014, 48:30-42.
58. Morgan J.A., Corrigan F., Baune B.T. Effects of physical exercise on central nervous system functions: a review of brain region specific adaptations. J Mol Psychiatry 2015, 3:3.
59. Muguruza C., Miranda-Azpiazu P., Diez-Alarcia R., Morentin B., Gonzalez-Maeso J., Callado L.F., Meana J.J. Evaluation of 5-HT and mGlu receptors in postmortem prefrontal cortex of subjects with major depressive disorder: effect of antidepressant treatment. Neuropharmacology 2014, 86C:311-318.
60. Nishikimi T., Maeda N., Matsuoka H. The role of natriuretic peptides in cardioprotection. Cardiovasc Res 2006, 69:318-328.
61. Park S.D., Yu S.H. The effects of Nordic and general walking on depression disorder patients' depression, sleep, and body composition. J Phy Ther Sci 2015, 27:2481-2485.
62. Patki G., Solanki N., Atrooz F., Allam F., Salim S. Depression, anxiety-like behavior and memory impairment are associated with increased oxidative stress and inflammation in a rat model of social stress. Brain Resh 2013, 1539:73-86.
63. Pedersen B.K., Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 2000, 80:1055-1081.
64. Prossin A.R., Koch A.E., Campbell P.L., McInnis M.G., Zalcman S.S., Zubieta J.-K. Association of plasma interleukin-18 levels with emotion regulation and μ-opioid neurotransmitter function in major depression and healthy volunteers. Biol. Psychiatry 2011, 69(8):808-812.
65. Radak Z., Chung H.Y., Goto S. Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic Biol Med 2008, 44:153-159.
66. Radak Z., Chung H.Y., Koltai E., Taylor A.W., Goto S. Exercise, oxidative stress and hormesis. Ageing Res Rev 2008, 7:34-42.
67. Radak Z., Taylor A.W., Ohno H., Goto S. Adaptation to exercise-induced oxidative stress: from muscle to brain. Exerc Immunol Rev 2001, 7:90-107.
68. Ransome M.I., Turnley A.M. Growth hormone signaling and hippocampal neurogenesis: insights from genetic models. Hippocampus 2008, 18:1034-1050.
69. Rethorst C.D., Toups M.S., Greer T.L., Nakonezny P.A., Carmody T.J., Grannemann B.D., Huebinger R.M., Barber R.C., Trivedi M.H. Pro-inflammatory cytokines as predictors of antidepressant effects of exercise in major depressive disorder. Mol Psychiatry 2013, 18:1119-1124.
70. Rethorst C.D., Wipfli B.M., Landers D.M. The antidepressive effects of exercise: a meta-analysis of randomized trials. Sports Med 2009, 39:491-511.
71. Rive M.M., van Rooijen G., Veltman D.J., Phillips M.L., Schene A.H., Ruhe H.G. Neural correlates of dysfunctional emotion regulation in major depressive disorder: a systematic review of neuroimaging studies. Neurosci Biobehav Rev 2013, 37:2529-2553.
72. Salehi I., Hosseini S.M., Haghighi M., Jahangard L., Bajoghli H., Gerber M., Puhse U., Kirov R., Holsboer-Trachsler E., Brand S. Electroconvulsive therapy and aerobic exercise training increased BDNF and ameliorated depressive symptoms in patients suffering from treatment-resistant major depressive disorder. J Psychiatr Res 2014, 57:117-124.
73. Sapolsky R.M. The possibility of neurotoxicity in the hippocampus in major depression: a primer on neuron death. Biol. Psychiatry 2000, 48(October (8)):755-765.
74. Scheewe T.W., van Haren N.E., Sarkisyan G., Schnack H.G., Brouwer R.M., de Glint M., Hulshoff Pol H.E., Backx F.J., Kahn R.S., Cahn W. Exercise therapy, cardiorespiratory fitness and their effect on brain volumes: a randomised controlled trial in patients with schizophrenia and healthy controls. Eur Neuropsychopharmacol 2013, 23:675-685.
75. Schildkraut J.J. The catecholamine hypothesis of affective disorders: a review of supporting evidence. Am J Psychiatry 1965, 122:509-522.
76. Schuch F.B., Vasconcelos-Moreno M.P., Borowsky C., Zimmermann A.B., Rocha N.S., Fleck M.P. Exercise and severe major depression: effect on symptom severity and quality of life at discharge in an inpatient cohort. J Psychiatr Res 2015, 61:25-32.
77. Schuch F.B., Vasconcelos-Moreno M.P., Borowsky C., Zimmermann A.B., Wollenhaupt-Aguiar B., Ferrari P., de Almeida Fleck M.P. The effects of exercise on oxidative stress (TBARS) and BDNF in severely depressed inpatients. Eur Arch Psychiatry Clin Neurosci 2014, 264(7):605-613.
78. Schüle C. Neuroendocrinological mechanisms of actions of antidepressant drugs. J Neuroendocrinol 2007, 19:213-226.
79. Silveira H., Deslandes A.C., de Moraes H., Mouta R., Ribeiro P., Piedade R., Laks J. Effects of exercise on electroencephalographic mean frequency in depressed elderly subjects. Neuropsychobiology 2010, 61:141-147.
80. Silveira H., Moraes H., Oliveira N., Coutinho E.S., Laks J., Deslandes A. Physical exercise and clinically depressed patients: a systematic review and meta-analysis. Neuropsychobiology 2013, 67:61-68.
81. Soares J.C., Mann J.J. The anatomy of mood disorders-review of structural neuroimaging studies. Biol Psychiatry 1997, 41:86-106.
82. Song C., Wang H. Cytokines mediated inflammation and decreased neurogenesis in animal models of depression. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35:760-768.
83. Sperner-Unterweger B., Kohl C., Fuchs D. Immune changes and neurotransmitters: possible interactions in depression?. Prog Neuropsychopharmacol Biol Psychiatry 2014, 48:268-276.
84. 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.
85. Steffens D.C., Krishnan K.R. Structural neuroimaging and mood disorders: recent findings, implications for classification, and future directions. Biol Psychiatry 1998, 43:705-712.
86. Toups M.S.P., Greer T.L., Kurian B.T., Grannemann B.D., Carmody T.J., Huebinger R., Rethorst C., Trivedi M.H. Effects of serum brain derived neurotrophic factor on exercise augmentation treatment of depression. J Psychiatric Res 2011, 45:1301-1306.
87. Valkanova V., Ebmeier K.P., Allan C.L. CRP, IL-6 and depression: a systematic review and meta-analysis of longitudinal studies. J Affect Disord 2013, 150:736-744.
88. Vancampfort D., Mitchell A.J., De Hert M., Sienaert P., Probst M., Buys R., Stubbs B. Type 2 diabetes in patients with major depressive disorder: a meta-analysis of prevalence estimates and predictors. Depress. Anxiety 2015, 32(October (10)):763-773.
89. Wegner M., Helmich I., Machado S., Nardi A.E., Arias-Carrion O., Budde H. Effects of exercise on anxiety and depression disorders: review of meta-analyses and neurobiological mechanisms. CNS Neurol Disord Drug Targets 2014, 13:1002-1014.
90. Willner P., Scheel-Krüger J., Belzung C. The neurobiology of depression and antidepressant action. Neurosci Biobehav Rev 2013, 37:2331-2371.
91. Wipfli B.M., Rethorst C.D., Landers D.M. The anxiolytic effects of exercise: a meta-analysis of randomized trials and dose-response analysis. J Sport Exerc Psychol 2008, 30:392-410.
92. Wisén A.G.M., Ekberg K., Wohlfart B., Ekman R., Westrin Å. Plasma ANP and BNP during exercise in patients with major depressive disorder and in healthy controls. J Affect Disord 2011, 129:371-375.
93. Zlatković J., Todorović N., Bošković M., Pajović S., Demajo M., Filipović D. Different susceptibility of prefrontal cortex and hippocampus to oxidative stress following chronic social isolation stress. Mol Cell Biochem 2014, 393:43-57.