The effects of motor rehabilitation training on clinical symptoms and serum BDNF levels in Parkinson’s disease subjects

Canadian Journal of Physiology and Pharmacology

Volumn 94, Issue 4, 2016, Pages 455-461

  Angelucci, Francesco ^a   Piermaria, Jacopo ^a   Gelfo, Francesca ^a,b   Shofany, Jacob ^a   Tramontano, Marco ^a   Fiore, Marco ^c   Caltagirone, Carlo ^a,b   Peppe, Antonella ^a  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c CNR   (Italy)

Author keywords

BDNF; Motor rehabilitation; Parkinson s disease; Physical exercise

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; LEVODOPA; BRAIN-DERIVED NEUROTROPHIC FACTOR, HUMAN;

ADULT; AGED; ARTICLE; BLOOD SAMPLING; BODY EQUILIBRIUM; BODY POSTURE; BREATHING; BREATHING EXERCISE; CLINICAL ARTICLE; CLINICAL PROTOCOL; DAILY LIFE ACTIVITY; DIAPHRAGM; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRAPYRAMIDAL SYMPTOM; FEMALE; FOLLOW UP; GAIT; HUMAN; JOINT MOBILITY; MALE; MIDDLE AGED; MOTOR COORDINATION; MOTOR FUNCTION TEST; MOTOR PERFORMANCE; MOTOR REHABILITATION; NECK; OUTCOME ASSESSMENT; PARKINSON DISEASE; PARKINSON DISEASE QUESTIONNAIRE 39; PATIENT MOBILITY; PHYSIOTHERAPY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; QUESTIONNAIRE; REHABILITATION CARE; RELAXATION TRAINING; RESISTANCE TRAINING; SIX MINUTE WALKING TEST; TREADMILL EXERCISE; UNIFIED PARKINSON DISEASE RATING SCALE; WALKING; BLOOD; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY; TEACHING; UPREGULATION;

ACTIVITIES OF DAILY LIVING; AGED; BRAIN-DERIVED NEUROTROPHIC FACTOR; FEMALE; GAIT; HUMANS; MALE; MIDDLE AGED; MOTOR ACTIVITY; PARKINSON DISEASE; PHYSICAL THERAPY MODALITIES; TEACHING; UP-REGULATION;

EID: 84964091501     PISSN: 00084212     EISSN: 12057541     Source Type: Journal    
DOI: 10.1139/cjpp-2015-0322     Document Type: Article

References (57)

1. Abbruzzese, G., Marchese, R., Avanzino, L., and Pelosin, E. 2016. Rehabilitation for Parkinson's disease: Current outlook and future challenges. Parkinsonism Relat. Disord. Suppl 1: S60-64. doi:10.1016/j.parkreldis.2015.09.005. PMID:26360239.
2. Ali, S.F., Binienda, Z.K., and Imam, S.Z. 2011. Molecular aspects of dopaminergic neurodegeneration: gene-environment interaction in parkin dysfunction. Int. J. Environ. Res. Public Health, 8(12): 4702-4713. doi:10.3390/ijerph8124702. PMID:22408597.
3. Angelucci, F., Ricci, V., Spalletta, G., Pomponi, M., Tonioni, F., Caltagirone, C., et al. 2008. Reduced serum concentrations of nerve growth factor, but not brain-derived neurotrophic factor, in chronic cannabis abusers. Eur. Neuropsychopharmacol. 18(12): 882-887. doi:10.1016/j.euroneuro.2008.07.008. PMID:18774699.
4. Barbieri, E., Agostini, D., Polidori, E., Potenza, L., Guescini, M., Lucertini, F., et al. 2015. The pleiotropic effect of physical exercise on mitochondrial dynamics in aging skeletal muscle. Oxid. Med. Cell. Longev. 2015: 917085. doi:10.1155/ 2015/917085. PMID:25945152.
5. Bekinschtein, P., Oomen, C.A., Saksida, L.M., and Bussey, T.J. 2011. Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable? Semin. Cell Dev. Biol. 22(5): 536-542. doi:10.1016/j.semcdb.2011.07.002. PMID:21767656.
6. Combs, S.A., Diehl, M.D., Filip, J., and Long, E. 2014. Short-distance walking speed tests in people with Parkinson disease: reliability, responsiveness, and validity. Gait Posture, 39(2): 784-788. doi:10.1016/j.gaitpost.2013.10.019. PMID: 24246801.
7. El-Tamawy, M.S., Abd-Allah, F., Ahmed, S.M., Darwish, M.H., and Khalifa, H.A. 2014. Aerobic exercises enhance cognitive functions and brain derived neurotrophic factor in ischemic stroke patients. NeuroRehabilitation, 34(1): 209-213. doi:10.3233/NRE-131020. PMID:24284463.
8. Folstein, M.F., Folstein, S.E., and McHugh, P.R. 1975. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12(3): 189-198. doi:10.1016/0022-3956(75)90026-6. PMID: 1202204.
9. Frazzitta, G., Bertotti, G., Uccellini, D., and Maestri, R. 2010. Parkinson's disease rehabilitation: a pilot study with 1 year follow up. Mov. Disord. 25(11): 1762-1763. doi:10.1002/mds.23316. PMID:20589873.
10. Frazzitta, G., Balbi, P., Maestri, R., Bertotti, G., Boveri, N., and Pezzoli, G. 2013. The beneficial role of intensive exercise on Parkinson disease progression. Am. J. Phys. Med. Rehabil. 92(6): 523-532. doi:10.1097/PHM.0b013e31828cd254. PMID:23552330.
11. Frazzitta, G., Maestri, R., Ghilardi, M.F., Riboldazzi, G., Perini, M., Bertotti, G., et al. 2014. Intensive Rehabilitation Increases BDNF Serum Levels in Parkinsonian Patients: A Randomized Study. Neurorehabil. Neural Repair, 28(2): 163-168. doi:10.1177/1545968313508474. PMID:24213955.
12. Frim, D.M., Uhler, T.A., Galpern, W.R., Beal, M.F., Breakefield, X.O., and Isacson, O. 1994. Implanted fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevent 1-methyl-4-phenylpyridinium toxicity to dopaminergic neurons in the rat. Proc. Natl. Acad. Sci. U.S.A. 91(11): 5104-5108. doi:10.1073/pnas.91.11.5104. PMID:8197193.
13. Garcia-Ruiz, P.J., Martinez, Castrillo, J.C., Alonso-Canovas, A., Herranz Barcenas, A., Vela, L., Sanchez Alonso, P., et al. 2014. Impulse control disorder in patients with Parkinson's disease under dopamine agonist therapy: a multicentre study. J. Neurol. Neurosurg. Psychiatry, 85(8): 840-844. doi:10.1136/jnnp-2013-306787. PMID:24434037.
14. Gazewood, J.D., Richards, D.R., and Clebak, K. 2013. Parkinson disease: an update. Am. Fam. Physician, 87(4): 267-273. PMID:23418798.
15. Gelb, D.J., Oliver, E., and Gilman, S. 1999. Diagnostic criteria for Parkinson disease. Arch. Neurol. 56(1): 33-39. doi:10.1001/archneur.56.1.33. PMID:9923759.
16. Gelfo, F., Cutuli, D., Foti, F., Laricchiuta, D., De Bartolo, P., Caltagirone, C., et al. 2011. Enriched environment improves motor function and increases neurotrophins in hemicerebellar lesioned rats. Neurorehabil. Neural Repair, 25(3): 243-252. doi:10.1177/1545968310380926. PMID:20966156.
17. Goetz, C.G., Poewe, W., Rascol, O., Sampaio, C., Stebbins, G.T., Counsell, C., et al. 2004. Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: status and recommendations. Mov. Disord. 19(9): 1020-1028. PMID:15372591.
18. Gómez-Palacio-Schjetnan, A, and Escobar, ML. 2013. Neurotrophins and synaptic plasticity. Curr. Top. Behav. Neurosci. 15: 117-136. doi:10.1007/7854_2012_231. PMID:23519767.
19. Guyatt, G.H., Sullivan, M.J., Thompson, P.J., Fallen, E.L., Pugsley, S.O., Taylor, D.W., et al. 1985. The 6-minute walk: a new measure of exercise capacity in patients with chronic heart failure. Can. Med. Assoc. J. 132(8): 919-923. PMID:3978515.
20. Gyárfás, T., Knuuttila, J., Lindholm, P., Rantamäki, T., and Castrén, E. 2010. Regulation of brain-derived neurotrophic factor (BDNF) and cerebral dopamine neurotrophic factor (CDNF) by anti-parkinsonian drug therapy in vivo. Cell. Mol. Neurobiol. 30(3): 361-368. doi:10.1007/s10571-009-9458-3. PMID: 19777340.
21. Huot, P., Johnston, T.H., Koprich, J.B., Fox, S.H., and Brotchie, J.M. 2013. The pharmacology of L-DOPA-induced dyskinesia in Parkinson's disease. Pharmacol. Rev. 65(1): 171-222. doi:10.1124/pr.111.005678. PMID:23319549.
22. Hyman, C., Hofer, M., Barde, Y.A., Juhasz, M., Yancopoulos, G.D., Squinto, S.P., et al. 1991. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature, 350(6315): 230-232. doi:10.1038/350230a0. PMID: 2005978.
23. Ji, Y., Lu, Y., Yang, F., Shen, W., Tang, T.T., Feng, L., et al. 2010. Acute and gradual increases in BDNF concentration elicit distinct signaling and functions in neurons. Nat. Neurosci. 13(3): 302-309. doi:10.1038/nn.2505. PMID:20173744.
24. Karege, F., Schwald, M., and Cisse, M. 2002. Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets. Neurosci. Lett. 328(3): 261-264. doi:10.1016/S0304-3940(02)00529-3. PMID:12147321.
25. Kleim, J.A., Jones, T.A., and Schallert, T. 2003. Motor enrichment and the induction of plasticity before or after brain injury. Neurochem. Res. 28(11): 1757-1769. doi:10.1023/A:1026025408742. PMID:14584829.
26. Knaepen, K., Goekint, M., Heyman, E.M,., and Meeusen, R. 2010. Neuroplasticity-exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects. Sports Med. 40(9): 765-801. doi:10.2165/11534530-000000000-00000. PMID:20726622.
27. Lau, Y.S., Patki, G., Das-Panja, K., Le, W.D., and Ahmad, S.O. 2011. Neuroprotective effects and mechanisms of exercise in a chronic mouse model of Parkinson's disease with moderate neurodegeneration. Eur. J. Neurosci. 33(7): 1264-1274. doi:10.1111/j.1460-9568.2011.07626.x. PMID:21375602.
28. Levivier, M., Przedborski, S., Bencsics, C., and Kang, U.J. 1995. Intrastriatal implantation of fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevents degeneration of dopaminergic neurons in a rat model of Parkinson's disease. J. Neurosci. 15(12): 7810-7820. PMID:8613721.
29. Lommatzsch, M., Zingler, D., Schuhbaeck, K., Schloetcke, K., Zingler, C., Schuff-Werner, P., et al. 2005. The impact of age, weight and gender on BDNF levels in human platelets and plasma. Neurobiol. Aging, 26(1): 115-123. doi: 10.1016/j.neurobiolaging.2004.03.002. PMID:15585351.
30. Maruyama, W., and Naoi, M. 2013. "70th Birthday Professor Riederer" induction of glial cell line-derived and brain-derived neurotrophic factors by rasagiline and (-)deprenyl: a way to a disease-modifying therapy? J. Neural Transm. 120(1): 83-89. doi:10.1007/s00702-012-0876-x. PMID:22892822.
31. McCullough, M.J., Gyorkos, A.M., and Spitsbergen, J.M. 2013. Short-term exercise increases GDNF protein levels in the spinal cord of young and old rats. Neuroscience, 240: 258-268. doi:10.1016/j.neuroscience.2013.02.063. PMID: 23500094.
32. Mehrholz, J., Friis, R., Kugler, J., Twork, S., Storch, A., and Pohl, M. 2010. Treadmill training for patients with Parkinson's disease. Cochrane Database Syst. Rev. 2010(1): CD007830. doi:10.1002/14651858.CD007830. PMID:20091652.
33. Mhatre, P.V., Vilares, I., Stibb, S.M., Albert, M.V., Pickering, L., Marciniak, C.M., et al. 2013. Wii Fit balance board playing improves balance and gait in Parkinson Disease. PM R, 5(9): 769-777. doi:10.1016/j.pmrj.2013.05.019. PMID: 23770422.
34. Michel, P.P., Toulorge, D., Guerreiro, S., and Hirsch, E.C. 2013. Specific needs of dopamine neurons for stimulation in order to survive: implication for Parkinson disease. FASEB J. 27(9): 3414-3423. doi:10.1096/fj.12-220418. PMID: 23699175.
35. Mogi, M., Togari, A., Kondo, T., Mizuno, Y., Komure, O., Kuno, S., et al. 1999. Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson's disease. Neurosci. Lett. 270(1): 45-48. doi:10.1016/S0304-3940(99)00463-2. PMID:10454142.
36. Movement Disorder Society Task Force on Rating Scales for Parkinson's Disease. 2003. The Unified Parkinson's Disease Rating Scale (UPDRS): status and recommendations. Mov. Disord. 18(7): 738-750. doi:10.1002/mds.10473. PMID: 12815652.
37. Pan, W., Banks, W.A., Fasold, M.B., Bluth, J., and Kastin, A.J. 1998. Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology, 37(12): 1553-1561. doi:10.1016/S0028-3908(98)00141-5. PMID: 9886678.
38. Parain, K., Murer, M.G., Yan, Q., Faucheux, B., Agid, Y., Hirsch, E., et al. 1999. Reduced expression of brain-derived neurotrophic factor protein in Parkinson's disease substantia nigra. Neuroreport, 10(3): 557-561. doi:10.1097/00001756-199902250-00021. PMID:10208589.
39. Peppe, A., Chiavalon, C., Pasqualetti, P., Crovato, D., and Caltagirone, C. 2007. Does gait analysis quantify motor rehabilitation efficacy in Parkinson's disease patients? Gait Posture, 26(3): 452-462. doi:10.1016/j.gaitpost.2006.11.207. PMID:17240143.
40. Pereira, D.S., de Queiroz, B.Z., Miranda, A.S., Rocha, N.P., Felício, D.C., Mateo, E.C., et al. 2013. Effects of physical exercise on plasma levels of brainderived neurotrophic factor and depressive symptoms in elderly women-a randomized clinical trial. Arch. Phys. Med. Rehabil. 94(8): 1443-1450. doi:10. 1016/j.apmr.2013.03.029. PMID:23602881.
41. Peto, V., Jenkinson, C., Fitzpatrick, R., and Greenhall, R. 1995. The development and validation of a short measure of functioning and well being for individuals with Parkinson's disease. Qual. Life Res. 4(3): 241-248. doi:10.1007/ BF02260863. PMID:7613534.
42. Poduslo, J.F., and Curran, G.L. 1996. Permeability at the blood-brain and bloodnerve barriers of the neurotrophic factors: NGF, CNTF, NT-3, BDNF. Brain Res. Mol. Brain Res. 36(2): 280-286. doi:10.1016/0169-328X(95)00250-V. PMID: 8965648.
43. Pompeu, J.E., dos Santos Mendes, F.A., da Silva, K.G., Lobo, A.M., de Paula Oliveira, T., Zomignani, A.P., et al. 2012. Effect of Nintendo Wii™-based motor and cognitive training on activities of daily living in patients with Parkinson's disease: a randomised clinical trial. Physiotherapy, 98(3): 196-204. doi:10.1016/j.physio.2012.06.004. PMID:22898575.
44. Rasmussen, P., Brassard, P., Adser, H., Pedersen, M.V., Leick, L., Hart, E., et al. 2009. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp. Physiol. 94(10): 1062-1069. doi:10.1113/expphysiol. 2009.048512. PMID:19666694.
45. Ricci, V., Pomponi, M., Martinotti, G., Bentivoglio, A., Loria, G., Bernardini, S., et al. 2010. Antidepressant treatment restores brain-derived neurotrophic factor serum levels and ameliorates motor function in Parkinson disease patients. J. Clin. Psychopharmacol. 30(6): 751-753. doi:10.1097/JCP.0b013e3181fc2ec7. PMID: 21057246.
46. Scalzo, P., Kümmer, A., Bretas, T.L., Cardoso, F., and Teixeira, A.L. 2010. Serum levels of brain-derived neurotrophic factor correlate with motor impairment in Parkinson's disease. J. Neurol. 257(4): 540-545. doi:10.1007/s00415-009-5357-2. PMID:19847468.
47. Schmolesky, M.T., Webb, D.L., and Hansen, R.A. 2013. The effects of aerobic exercise intensity and duration on levels of brain-derived neurotrophic factor in healthy men. J. Sports Sci. Med. 12(3): 502-511. PMID:24149158.
48. Sharma, A., Goyal, V., Behari, M., Srivastva, A., Shukla, G., and Vibha, D. 2015. Impulse control disorders and related behaviours (ICD-RBs) in Parkinson's disease patients: Assessment using "Questionnaire for impulsive-compulsive disorders in Parkinson's disease" (QUIP). Ann. Indian Acad. Neurol. 18(1): 49-59. doi:10.4103/0972-2327.144311. PMID:25745311.
49. Tomlinson, C.L., Patel, S., Meek, C., Herd, C.P., Clarke, C.E., Stowe, R., et al. 2013. Physiotherapy versus placebo or no intervention in Parkinson's disease. Cochrane Database Syst. Rev. 2013(9): CD002817. doi:10.1002/14651858. CD002817. PMID:24018704.
50. Tsukahara, T., Takeda, M., Shimohama, S., Ohara, O., and Hashimoto, N. 1995. Effects of brain-derived neurotrophic factor on 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-induced parkinsonism in monkeys. Neurosurgery, 37: 733-741. doi:10.1227/00006123-199510000-00018. PMID:8559303.
51. Vassar, S.D., Bordelon, Y.M., Hays, R.D., Diaz, N., Rausch, R., Mao, C., et al. 2012. Confirmatory factor analysis of the motor unified Parkinson's disease rating scale. Parkinsons Dis. 2012: 719167. doi:10.1155/2012/719167. PMID:23133789.
52. Vaughan, S,., Wallis, M., Polit, D., Steele, M., Shum, D., and Morris, N. 2014. The effects of multimodal exercise on cognitive and physical functioning and brain-derived neurotrophic factor in older women: a randomised controlled trial. Age Ageing, 43(5): 623-629. doi:10.1093/ageing/afu010. PMID:24554791.
53. Weintraub, D., Hoops, S., Shea, J.A., Lyons, K.E., Pahwa, R., Driver-Dunckley, E.D., et al. 2009. Validation of the questionnaire for impulsive-compulsive disorders in Parkinson's disease. Mov. Disord. 24(10): 1461-1467. doi:10.1002/mds.22571. PMID:19452562.
54. Wilcox, R.R. 1987. New Statistical Procedures for the Social Sciences. Erlbaum: Hillsdale, New Jersey.
55. Worth, P.F. 2013. How to treat Parkinson's disease in 2013. Clin. Med. 13(1): 93-96. doi:10.7861/clinmedicine.13-1-93. PMID:23472504.
56. Zhang, J.L., and Chan, P. 2012. Reliability and validity of PDQ-39: a quality-of-life measure for patients with PD in China. Qual. Life Res. 21(7): 1217-1221. doi: 10.1007/s11136-011-0026-1. PMID:21983714.
57. Ziebell, M., Khalid, U., Klein, A.B., Aznar, S., Thomsen, G., Jensen, P., et al. 2012. Striatal dopamine transporter binding correlates with serum BDNF levels in patients with striatal dopaminergic neurodegeneration. Neurobiol. Aging, 33(2): 428.e1-5. doi:10.1016/j.neurobiolaging.2010.11.010. PMID:21176997.