Exercise-induced increase in brain-derived neurotrophic factor in human Parkinson's disease: a systematic review and meta-analysis

Mark A Hirsch, Erwin E H van Wegen, Mark A Newman, Patricia C Heyn, Mark A Hirsch, Erwin E H van Wegen, Mark A Newman, Patricia C Heyn

Abstract

Background: Animal models of exercise and Parkinson's disease (PD) have found that the physiologic use of exercise may interact with the neurodegenerative disease process, likely mediated by brain derived neurotrophic factor (BDNF). No reviews so far have assessed the methodologic quality of available intervention studies or have bundled the effect sizes of individual studies on exercise-induced effects on BDNF blood levels in human PD.

Research design and methods: We searched MEDLINE, EMBASE, Cochrane Library, PsycINFO and PubMed from inception to June 2017.

Results: Data aggregated from two randomized controlled trials and four pre-experimental studies with a total of 100 ambulatory patients with idiopathic PD (Hoehn/Yahr ≤3) found improvements in BDNF blood concentration levels in all 6 studies (two RCTs and 4 pre-experimental studies). Pooled BDNF level change scores from the 2 RCTs resulted in a significant homogeneous summary effect size (Standardized Mean Difference 2.06, 95% CI 1.36 to 2.76), and a significant heterogeneous SES for the motor part of the UPDRS-III examination (MD -5.53, 95% CI -10.42 to -0.64). Clinical improvements were noted in all studies using a variety of outcome measures.

Limitations: The evidence-base consists primarily of small studies with low to moderate methodological quality.

Conclusions: This review provides preliminary evidence for the effectiveness of physical exercise treatments for persons with PD on BDNF blood levels. Further research is needed.

Keywords: Brain derived neurotrophic factor; Exercise; Parkinson’s disease; Rehabilitation; Systematic review.

Conflict of interest statement

Not applicable.Not applicable.The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
PRISMA flow diagram
Fig. 2
Fig. 2
Summary effect sizes for outcome of change in BDNF levels. Green squares indicate individual SES. Black colored diamond indicates the summary effect size; RCT randomized clinical trial, SD standard deviation, Std standardized, CI Confidence Interval, I2 statistic to determine heterogeneity, Z z-score
Fig. 3
Fig. 3
Summary effect sizes for outcome of change in MDS-UPDRS motor score. Green squares indicate individual SES. Black colored diamond indicates the summary effect size; RCT randomized clinical trial, SD standard deviation, CI Confidence Interval, I2 statistic to determine heterogeneity, Z z-score

References

    1. Kalia LV, Lang AE. Parkinson's disease. Lancet. 2015;386:896–912. doi: 10.1016/S0140-6736(14)61393-3.
    1. Cascaes da Silva F, Iop Rda R, Domingos dos Santos P, Aguiar Bezerra de Melo LM, Barbosa Gutierres Filho PJ, da Silva R. Effects of Physical-Exercise-Based Rehabilitation Programs on the Quality of Life of Patients With Parkinson's Disease: A Systematic Review of Randomized Controlled Trials. J Aging Phys Act. 2016;24:484–496. doi: 10.1123/japa.2015-0162.
    1. Lauze M, Daneault JF, Duval C. The Effects of Physical Activity in Parkinson's Disease: A Review. J Parkinsons Dis. 2016;6:685–698. doi: 10.3233/JPD-160790.
    1. Munneke M, Nijkrake MJ, Keus SH, Kwakkel G, Berendse HW, Roos RA, Borm GF, Adang EM, Overeem S, Bloem BR. Efficacy of community-based physiotherapy networks for patients with Parkinson's disease: a cluster-randomised trial. Lancet Neurol. 2010;9:46–54. doi: 10.1016/S1474-4422(09)70327-8.
    1. Petzinger GM, Fisher BE, McEwen S, Beeler JA, Walsh JP, Jakowec MW. Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease. Lancet Neurol. 2013;12:716–726. doi: 10.1016/S1474-4422(13)70123-6.
    1. Ridgel AL, Walter BL, Tatsuoka C, Walter EM, Colon-Zimmermann K, Welter E, Sajatovic M. Enhanced Exercise Therapy in Parkinson's disease: A comparative effectiveness trial. J Sci Med Sport. 2016;19:12–17. doi: 10.1016/j.jsams.2015.01.005.
    1. Saltychev M, Barlund E, Paltamaa J, Katajapuu N, Laimi K. Progressive resistance training in Parkinson's disease: a systematic review and meta-analysis. BMJ Open. 2016;6:e008756. doi: 10.1136/bmjopen-2015-008756.
    1. Schenkman M, Hall DA, Baron AE, Schwartz RS, Mettler P, Kohrt WM. Exercise for people in early- or mid-stage Parkinson disease: a 16-month randomized controlled trial. Phys Ther. 2012;92:1395–1410. doi: 10.2522/ptj.20110472.
    1. Tomlinson CL, Herd CP, Clarke CE, Meek C, Patel S, Stowe R, Deane KH, Shah L, Sackley CM, Wheatley K, Ives N. Physiotherapy for Parkinson's disease: a comparison of techniques. Cochrane Database Syst Rev. 2014:Cd002815.
    1. Ahlskog JE. Does vigorous exercise have a neuroprotective effect in Parkinson disease. Neurology. 2011;77:288–294. doi: 10.1212/WNL.0b013e318225ab66.
    1. Hirsch MA, Farley BG. Exercise, neuroplasticity and Parkinson’s disease. Eur J Phys Rehabil Med. 2009;45(2):215–29.
    1. Fisher BE, Petzinger GM, Nixon K, Hogg E, Bremmer S, Meshul CK, Jakowec MW. Exercise-induced behavioral recovery and neuroplasticity in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse basal ganglia. J Neurosci Res. 2004;77:378–390. doi: 10.1002/jnr.20162.
    1. Petzinger GM, Walsh JP, Akopian G, Hogg E, Abernathy A, Arevalo P, Turnquist P, Vuckovic M, Fisher BE, Togasaki DM, Jakowec MW. Effects of treadmill exercise on dopaminergic transmission in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse model of basal ganglia injury. J Neurosci. 2007;27:5291–5300. doi: 10.1523/JNEUROSCI.1069-07.2007.
    1. Tajiri N, Yasuhara T, Shingo T, Kondo A, Yuan W, Kadota T, Wang F, Baba T, Tayra JT, Morimoto T, et al. Exercise exerts neuroprotective effects on Parkinson's disease model of rats. Brain Res. 2010;1310:200–207. doi: 10.1016/j.brainres.2009.10.075.
    1. Alexi T, Hefti F. Neurotrophin-4/5 selectively protects nigral calbindin-containing neurons in rats with medial forebrain bundle transections. Neuroscience. 1996;72:911–921. doi: 10.1016/0306-4522(95)00607-9.
    1. Cohen AD, Tillerson JL, Smith AD, Schallert T, Zigmond MJ. Neuroprotective effects of prior limb use in 6-hydroxydopamine-treated rats: possible role of GDNF. J Neurochem. 2003;85:299–305. doi: 10.1046/j.1471-4159.2003.01657.x.
    1. Daviaud N, Garbayo E, Sindji L, Martinez-Serrano A, Schiller PC, Montero-Menei CN. Survival, differentiation, and neuroprotective mechanisms of human stem cells complexed with neurotrophin-3-releasing pharmacologically active microcarriers in an ex vivo model of Parkinson's disease. Stem Cells Transl Med. 2015;4:670–684. doi: 10.5966/sctm.2014-0139.
    1. Gu S, Huang H, Bi J, Yao Y, Wen T. Combined treatment of neurotrophin-3 gene and neural stem cells is ameliorative to behavior recovery of Parkinson's disease rat model. Brain Res. 2009;1257:1–9. doi: 10.1016/j.brainres.2008.12.016.
    1. Jiang P, Dang RL, Li HD, Zhang LH, Zhu WY, Xue Y, Tang MM. The impacts of swimming exercise on hippocampal expression of neurotrophic factors in rats exposed to chronic unpredictable mild stress. Evid Based Complement Alternat Med. 2014;2014:729827.
    1. Jung SY, Kim DY, Yune TY, Shin DH, Baek SB, Kim CJ. Treadmill exercise reduces spinal cord injury-induced apoptosis by activating the PI3K/Akt pathway in rats. Exp Ther Med. 2014;7:587–593. doi: 10.3892/etm.2013.1451.
    1. Koo HM, Lee SM, Kim MH. Spontaneous Wheel Running Exercise Induces Brain Recovery via Neurotrophin-3 Expression Following Experimental Traumatic Brain Injury in Rats. J Phys Ther Sci. 2013;25:1103–1107. doi: 10.1589/jpts.25.1103.
    1. Real CC, Ferreira AF, Chaves-Kirsten GP, Torrao AS, Pires RS, Britto LR. BDNF receptor blockade hinders the beneficial effects of exercise in a rat model of Parkinson's disease. Neuroscience. 2013;237:118–129. doi: 10.1016/j.neuroscience.2013.01.060.
    1. Sauer H, Wong V, Bjorklund A. Brain-derived neurotrophic factor and neurotrophin-4/5 modify neurotransmitter-related gene expression in the 6-hydroxydopamine-lesioned rat striatum. Neuroscience. 1995;65:927–933. doi: 10.1016/0306-4522(95)00019-F.
    1. Sharma NK, Ryals JM, Gajewski BJ, Wright DE. Aerobic exercise alters analgesia and neurotrophin-3 synthesis in an animal model of chronic widespread pain. Phys Ther. 2010;90:714–725. doi: 10.2522/ptj.20090168.
    1. Woodlee MT, Schallert T. The interplay between behavior and neurodegeneration in rat models of Parkinson's disease and stroke. Restor Neurol Neurosci. 2004;22:153–161.
    1. Wu SY, Wang TF, Yu L, Jen CJ, Chuang JI, Wu FS, Wu CW, Kuo YM. Running exercise protects the substantia nigra dopaminergic neurons against inflammation-induced degeneration via the activation of BDNF signaling pathway. Brain Behav Immun. 2011;25:135–146. doi: 10.1016/j.bbi.2010.09.006.
    1. Ying Z, Roy RR, Edgerton VR, Gomez-Pinilla F. Exercise restores levels of neurotrophins and synaptic plasticity following spinal cord injury. Exp Neurol. 2005;193:411–419. doi: 10.1016/j.expneurol.2005.01.015.
    1. Zigmond MJ, Exercise SRJ. is it a neuroprotective and if so, how does it work? Parkinsonism Relat Disord. 2014;20(Suppl 1):S123–S127. doi: 10.1016/S1353-8020(13)70030-0.
    1. 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;40:765–801. doi: 10.2165/11534530-000000000-00000.
    1. 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.
    1. Vaynman S, Gomez-Pinilla F. License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabil Neural Repair. 2005;19:283–295. doi: 10.1177/1545968305280753.
    1. Castellano V, White LJ. Serum brain-derived neurotrophic factor response to aerobic exercise in multiple sclerosis. J Neurol Sci. 2008;269:85–91. doi: 10.1016/j.jns.2007.12.030.
    1. Gold SM, Schulz KH, Hartmann S, Mladek M, Lang UE, Hellweg R, Reer R, Braumann KM, Heesen C. Basal serum levels and reactivity of nerve growth factor and brain-derived neurotrophic factor to standardized acute exercise in multiple sclerosis and controls. J Neuroimmunol. 2003;138:99–105. doi: 10.1016/S0165-5728(03)00121-8.
    1. 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;16:960–972. doi: 10.1038/mp.2010.88.
    1. Vinogradov S, Fisher M, Holland C, Shelly W, Wolkowitz O, Mellon SH. Is serum brain-derived neurotrophic factor a biomarker for cognitive enhancement in schizophrenia. Biol Psychiatry. 2009;66:549–553. doi: 10.1016/j.biopsych.2009.02.017.
    1. Gomez-Pinilla F, Zhuang Y, Feng J, Ying Z, Fan G. Exercise impacts brain-derived neurotrophic factor plasticity by engaging mechanisms of epigenetic regulation. Eur J Neurosci. 2011;33:383–390. doi: 10.1111/j.1460-9568.2010.07508.x.
    1. Ahlskog JE, Geda YE, Graff-Radford NR, Petersen RC. Physical exercise as a preventive or disease-modifying treatment of dementia and brain aging. Mayo Clin Proc. 2011;86:876–884. doi: 10.4065/mcp.2011.0252.
    1. Murer MG, 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. doi: 10.1016/S0301-0082(00)00014-9.
    1. Neeper SA, Gomez-Pinilla F, Choi J, Cotman C. Exercise and brain neurotrophins. Nature. 1995;373:109. doi: 10.1038/373109a0.
    1. Zuccato C, Cattaneo E. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat Rev Neurol. 2009;5:311–322. doi: 10.1038/nrneurol.2009.54.
    1. Campos C, Rocha NB, Lattari E, Paes F, Nardi AE, Machado S. Exercise-induced neuroprotective effects on neurodegenerative diseases: the key role of trophic factors. Expert Rev Neurother. 2016;16:723–734. doi: 10.1080/14737175.2016.1179582.
    1. da Silva PG, Domingues DD, de Carvalho LA, Allodi S, Correa CL. Neurotrophic factors in Parkinson's disease are regulated by exercise: Evidence-based practice. J Neurol Sci. 2016;363:5–15. doi: 10.1016/j.jns.2016.02.017.
    1. Hirsch MA, Hirsch HVB. The Adaptable Brain: Biology of Social Neuroplasticity. Topics in Geriatric Rehabilitation. 2014;30:2–7. doi: 10.1097/TGR.0000000000000003.
    1. Razgado-Hernandez LF, Espadas-Alvarez AJ, Reyna-Velazquez P, Sierra-Sanchez A, Anaya-Martinez V, Jimenez-Estrada I, Bannon MJ, Martinez-Fong D, Aceves-Ruiz J. The transfection of BDNF to dopamine neurons potentiates the effect of dopamine D3 receptor agonist recovering the striatal innervation, dendritic spines and motor behavior in an aged rat model of Parkinson's disease. PLoS One. 2015;10:e0117391. doi: 10.1371/journal.pone.0117391.
    1. Fumagalli F, Racagni G, Riva MA. Shedding light into the role of BDNF in the pharmacotherapy of Parkinson's disease. Pharmacogenomics J. 2006;6:95–104. doi: 10.1038/sj.tpj.6500360.
    1. Nam JH, Leem E, Jeon MT, Jeong KH, Park JW, Jung UJ, Kholodilov N, Burke RE, Jin BK, Kim SR. Induction of GDNF and BDNF by hRheb(S16H) transduction of SNpc neurons: neuroprotective mechanisms of hRheb(S16H) in a model of Parkinson's disease. Mol Neurobiol. 2015;51:487–499. doi: 10.1007/s12035-014-8729-2.
    1. Markham A, Bains R, Franklin P, Spedding M. Changes in mitochondrial function are pivotal in neurodegenerative and psychiatric disorders: how important is BDNF? Br J Pharmacol. 2014;171:2206–2229. doi: 10.1111/bph.12531.
    1. Yang JL, Lin YT, Chuang PC, Bohr VA, Mattson MP. BDNF and exercise enhance neuronal DNA repair by stimulating CREB-mediated production of apurinic/apyrimidinic endonuclease 1. Neuromolecular Med. 2014;16:161–174. doi: 10.1007/s12017-013-8270-x.
    1. Fox SH, Katzenschlager R, Lim SY, Ravina B, Seppi K, Coelho M, Poewe W, Rascol O, Goetz CG, Sampaio C. The Movement Disorder Society Evidence-Based Medicine Review Update: Treatments for the motor symptoms of Parkinson's disease. Mov Disord. 2011;26(Suppl 3):S2–41. doi: 10.1002/mds.23829.
    1. Keus SHJ, Munneke M, Graziano M. European Physiotherapy Guideline for Parkinson's disease. KNGF/ParkinsonNet: The Netherlands; 2014.
    1. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097. doi: 10.1371/journal.pmed.1000097.
    1. Heyn P, Abreu BC, Ottenbacher KJ. The effects of exercise training on elderly persons with cognitive impairment and dementia: a meta-analysis. Arch Phys Med Rehabil. 2004;85:1694–1704. doi: 10.1016/j.apmr.2004.03.019.
    1. Review Manager (RevMan) [Computer Program] The Cochrane Collaboration. Copenhagen: The Nordic Cochrane Centre; 2014.
    1. Lim I, van Wegen E, de Goede C, Deutekom M, Nieuwboer A, Willems A, Jones D, Rochester L, Kwakkel G. Effects of external rhythmical cueing on gait in patients with Parkinson's disease: a systematic review. Clin Rehabil. 2005;19:695–713. doi: 10.1191/0269215505cr906oa.
    1. Tooth LR, Ottenbacher KJ. The kappa statistic in rehabilitation research: an examination. Arch Phys Med Rehabil. 2004;85:1371–1376. doi: 10.1016/j.apmr.2003.12.002.
    1. Frazzitta G, Maestri R, Ghilardi MF, Riboldazzi G, Perini M, Bertotti G, Boveri N, Buttini S, Lombino FL, Uccellini D, et al. Intensive rehabilitation increases BDNF serum levels in parkinsonian patients: a randomized study. Neurorehabil Neural Repair. 2014;28:163–168. doi: 10.1177/1545968313508474.
    1. Sajatovic M, Ridgel AL, Walter EM, Tatsuoka CM, Colon-Zimmermann K, Ramsey RK, Welter E, Gunzler SA, Whitney CM, Walter BL. A randomized trial of individual versus group-format exercise and self-management in individuals with Parkinson's disease and comorbid depression. Patient Prefer Adherence. 2017;11:965–973. doi: 10.2147/PPA.S135551.
    1. Cohen J. Statistical Power Analysis for the Behavioral Sciences. 2. Hillsdale, NJ: Lawrence Erlbaum; 1988.
    1. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011.
    1. Fontanesi C, Kvint S, Frazzitta G, Bera R, Ferrazzoli D, Di Rocco A, Rebholz H, Friedman E, Pezzoli G, Quartarone A, et al. Intensive Rehabilitation Enhances Lymphocyte BDNF-TrkB Signaling in Patients With Parkinson's Disease. Neurorehabil Neural Repair. 2016;30:411–418. doi: 10.1177/1545968315600272.
    1. Zoladz JA, Majerczak J, Zeligowska E, Mencel J, Jaskolski A, Jaskolska A, Marusiak J. Moderate-intensity interval training increases serum brain-derived neurotrophic factor level and decreases inflammation in Parkinson's disease patients. J Physiol Pharmacol. 2014;65:441–448.
    1. Marusiak J, Zeligowska E, Mencel J, Kisiel-Sajewicz K, Majerczak J, Zoladz JA, Jaskolski A, Jaskolska A. Interval training-induced alleviation of rigidity and hypertonia in patients with Parkinson's disease is accompanied by increased basal serum brain-derived neurotrophic factor. J Rehabil Med. 2015;47:372–375. doi: 10.2340/16501977-1931.
    1. Angelucci F, Piermaria J, Gelfo F, Shofany J, Tramontano M, Fiore M, Caltagirone C, Peppe A. The effects of motor rehabilitation training on clinical symptoms and serum BDNF levels in Parkinson's disease subjects. Can J Physiol Pharmacol. 2016;94:455–461. doi: 10.1139/cjpp-2015-0322.
    1. Archer T. Influence of physical exercise on traumatic brain injury deficits: scaffolding effect. Neurotox Res. 2012;21:418–434. doi: 10.1007/s12640-011-9297-0.
    1. El-Tamawy MS, Abd-Allah F, Ahmed SM, Darwish MH, Khalifa HA. Aerobic exercises enhance cognitive functions and brain derived neurotrophic factor in ischemic stroke patients. NeuroRehabilitation. 2014;34:209–213.
    1. Lahera G, Bayon C, Fe Bravo-Ortiz M, Rodriguez-Vega B, Barbeito S, Saenz M, Avedillo C, Villanueva R, Ugarte A, Gonzalez-Pinto A, de Dios C. Mindfulness-based cognitive therapy versus psychoeducational intervention in bipolar outpatients with sub-threshold depressive symptoms: a randomized controlled trial. BMC Psychiatry. 2014;14:215. doi: 10.1186/s12888-014-0215-x.
    1. Horvath K, Aschermann Z, Acs P, Deli G, Janszky J, Komoly S, Balazs E, Takacs K, Karadi K, Kovacs N. Minimal clinically important difference on the Motor Examination part of MDS-UPDRS. Parkinsonism Relat Disord. 2015;21:1421–1426. doi: 10.1016/j.parkreldis.2015.10.006.
    1. 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;19:791–800. doi: 10.1038/mp.2013.105.
    1. Polacchini A, Metelli G, Francavilla R, Baj G, Florean M, Mascaretti LG, Tongiorgi E. A method for reproducible measurements of serum BDNF: comparison of the performance of six commercial assays. Sci Rep. 2015;5:17989. doi: 10.1038/srep17989.
    1. Bus BA, Molendijk ML, Penninx BJ, Buitelaar JK, Kenis G, Prickaerts J, Elzinga BM, Voshaar RC. Determinants of serum brain-derived neurotrophic factor. Psychoneuroendocrinology. 2011;36:228–239. doi: 10.1016/j.psyneuen.2010.07.013.
    1. Katoh-Semba R, Wakako R, Komori T, Shigemi H, Miyazaki N, Ito H, Kumagai T, Tsuzuki M, Shigemi K, Yoshida F, Nakayama A. Age-related changes in BDNF protein levels in human serum: differences between autism cases and normal controls. Int J Dev Neurosci. 2007;25:367–372. doi: 10.1016/j.ijdevneu.2007.07.002.
    1. El-Gharbawy AH, Adler-Wailes DC, Mirch MC, Theim KR, Ranzenhofer L, Tanofsky-Kraff M, Yanovski JA. Serum brain-derived neurotrophic factor concentrations in lean and overweight children and adolescents. J Clin Endocrinol Metab. 2006;91:3548–3552. doi: 10.1210/jc.2006-0658.
    1. Hashimoto K, Iwata Y, Nakamura K, Tsujii M, Tsuchiya KJ, Sekine Y, Suzuki K, Minabe Y, Takei N, Iyo M, Mori N. Reduced serum levels of brain-derived neurotrophic factor in adult male patients with autism. Prog Neuropsychopharmacol Biol Psychiatry. 2006;30:1529–1531. doi: 10.1016/j.pnpbp.2006.06.018.
    1. Fernandes BS, Gama CS, Cereser KM, Yatham LN, Fries GR, Colpo G, de Lucena D, Kunz M, Gomes FA, Kapczinski F. Brain-derived neurotrophic factor as a state-marker of mood episodes in bipolar disorders: a systematic review and meta-regression analysis. J Psychiatr Res. 2011;45:995–1004. doi: 10.1016/j.jpsychires.2011.03.002.
    1. Bocchio-Chiavetto L, Bagnardi V, Zanardini R, Molteni R, Nielsen MG, Placentino A, Giovannini C, Rillosi L, Ventriglia M, Riva MA, Gennarelli M. Serum and plasma BDNF levels in major depression: a replication study and meta-analyses. World J Biol Psychiatry. 2010;11:763–773. doi: 10.3109/15622971003611319.
    1. Scalzo P, Kummer A, Bretas TL, Cardoso F, Teixeira AL. Serum levels of brain-derived neurotrophic factor correlate with motor impairment in Parkinson’s disease. Journal of Neurology. 2010;257:540–545. doi: 10.1007/s00415-009-5357-2.
    1. Ventriglia M, Zanardini R, Bonomini C, Zanetti O, Volpe D, Pasqualetti P, Gennarelli M, Bocchio-Chiavetto L. Serum brain-derived neurotrophic factor levels in different neurological diseases. Biomed Research International. 2013. Article ID 901082. 10.1155/2013/901082.
    1. Bos I, Jacobs L, Nawrot TS, de Geus B, Torfs R, Panis LI, Degraeuwe B, Meeusen R. No exercise-induced increase in serum BDNF after cycling near a major traffic road. Neuroscience Letters. 2011;500(2):129. doi: 10.1016/j.neulet.2011.06.019.
    1. Bousquet M, Gibrat C, Saint-Pierre M, Julien C, Calon F, Cicchetti F. Modulation of brain-derived neurotrophic factor as a potential neuroprotective mechanism of action of omega-3 fatty acids in a parkinsonian animal model. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33(9):1401–1408. doi: 10.1016/j.pnpbp.2009.07.018.
    1. He J, Xiang Z, Zhu X, Ai Z, Shen J, Huang T, Liu L, Ji W, Li T. Neuroprotective effects of 7, 8-dihydroxylflavone on midbrain dopaminergic neurons in MPP+-treated monkeys. Sci Rep. 2016;6:34339. doi: 10.1038/srep34339.
    1. Van der Kolk NM, Speelman AD, van Nimwegen M, Kessels RP, IntHout J, Hakobjan M, Munneke M, Bloem BR, van de Warrenburg BP. BDNF polymorphism associates with decline in set shifting in Parkinson's disease. Neurobiol Aging. 2015;36:1605.e1601-e1606.
    1. Mougeot JL, Hirsch MA, Stevens CB, Mougeot F. Oral biomarkers in exercise-induced neuroplasticity in Parkinson's disease. Oral Dis. 2016;22:745–753. doi: 10.1111/odi.12463.
    1. Polacchini A, Metelli G, Francavilla R, Baj G, Florean M, Mascaretti LG, Tongiorgi E. A method for reproducible measurements of serum BDNF: comparison of the performance of six commercial assays. Scientific Reports. 2015;5:17989. doi: 10.1038/srep17989.
    1. Daviet JC, Roy X, Quelven-Bertin I, Jallageas R, Mandigout S, Torny F, Monteil J. Parkinson's patient runs an ultra marathon: a case report. Eur J Phys Rehabil Med. 2014;50:447–451.
    1. Piepmeier AT, Etnier JL. Brain-derived neurotrophic factor (BDNF) as a potential mechanism of the effects of acute exercise on cognitive performance. Journal of Sport and Health Science. 2015;4(1):14–23. doi: 10.1016/j.jshs.2014.11.001.
    1. Francardo V, Schmitz Y, Sulzer D, Cenci MA. Neuroprotection and neurorestoration as experimental therapeutics for Parkinson’s disease. Experimental Neurology. 2017;298:137–147. doi: 10.1016/j.expneurol.2017.10.001.
    1. Rimmer JH, Chen MD, McCubbin JA, Drum C, Peterson J. Exercise intervention research on persons with disabilities: what we know and where we need to go. Am J Phys Med Rehabil. 2010;89:249–263. doi: 10.1097/PHM.0b013e3181c9fa9d.
    1. Morris SB, DeShon RP. Combining effect size estimates in meta-analysis with repeated measures and independent-group designs. Psychological Methods. 2002;7(1):N–25. doi: 10.1037/1082-989X.7.1.105.

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