Biochemical markers of physical exercise on mild cognitive impairment and dementia: Systematic review and perspectives

Frontiers in Neurology

Volumn 6, Issue Aug, 2015, Pages

  Jensen, Camilla Steen ^a   Hasselbalch, Steen Gregers ^a,b   Waldemar, Gunhild ^a,b   Simonsen, Anja Hviid ^a  

^a Rigshospitalet   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Biomarkers; Dementia; Exercise intervention; MCI; Physical activity

Indexed keywords

BIOCHEMICAL MARKER; BRAIN DERIVED NEUROTROPHIC FACTOR; CHOLESTEROL; ESTRADIOL; INSULIN; PRASTERONE; TESTOSTERONE;

AEROBIC EXERCISE; CHOLESTEROL BLOOD LEVEL; COGNITION; DEMENTIA; EXECUTIVE FUNCTION; EXERCISE INTENSITY; HEART RATE; HORMONAL REGULATION; HORMONE BLOOD LEVEL; HUMAN; KINESIOTHERAPY; MILD COGNITIVE IMPAIRMENT; MINI MENTAL STATE EXAMINATION; OUTCOME ASSESSMENT; PROTEIN BLOOD LEVEL; RESISTANCE TRAINING; REVIEW; STRETCHING EXERCISE; SYSTEMATIC REVIEW; THERAPY EFFECT; TREATMENT DURATION; WALKING;

EID: 84940975339     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2015.00187     Document Type: Review

References (78)

1. Alzheimer's Disease International. Policy Brief for Heads of Government: The Global Impact of Dementia. London: Alzheimer's Disease International (2013). p. 2013-50.
2. Brookmeyer R, Johnson E, Ziegler-Graham K, Arrighi H. Forecasting the global burden of Alzheimer's disease. Alzheimers Dement (2007) 3:186-9. doi:10.1016/j.jalz.2007.04.381
3. Thies W, Bleiler L. 2013 Alzheimer's disease facts and figures. Alzheimers Dement (2013) 9:208-45. doi:10.1016/j.jalz.2013.02.003
4. Raina P, Santaguide P, Ismaila A, Patterson C, Cowan D, Levine M, et al. Effectiveness of cholinesterase inhibitor and memantine for treating dementia: evidence review for a clinical practive guideline. Ann Intern Med (2008) 148:379-97. doi:10.7326/0003-4819-148-5-200803040-00009
5. Sink KM, Holden KF, Yaffe K. Pharmacological treatment of neuropsychiatric symptoms of dementia: a review of the evidence. JAMA (2005) 293:596-608. doi:10.1001/jama.293.5.596
6. Mölsä P, Marttila R, Rinne U. Long-term survival and prediction of mortality in Alzheimer's disease and multi-infarct dementia. Acta Neurol Scand (1995) 91:159-64. doi:10.1111/j.1600-0404.1995.tb00426.x
7. Andel R, Crowe M, Pedersen NL, Fratiglioni L, Johansson B, Gatz M. Physical exercise at midlife and risk of dementia three decades later: a population-based study of Swedish twins. J Gerontol A Biol Sci Med Sci (2008) 63:62-6. doi:10.1093/gerona/63.1.62
8. Nyberg J, Åberg MAI, Schiöler L, Nilsson M, Wallin A, Torén K, et al. Cardiovascular and cognitive fitness at age 18 and risk of early-onset dementia. Brain (2014) 137:1514-23. doi:10.1093/brain/awu041
9. Lytle ME, Vander Bilt J, Pandav RS, Dodge HH, Ganguli M. Exercise level and cognitive decline: the MoVIES Project. Alzheimer Dis Assoc Disord (2004) 18:57-64. doi:10.1097/01.wad.0000126614.87955.79
10. Winchester J, DIck M, Gillen D, Reed B, Miller B, Tinklenberg J, et al. Walking stabilizes cognitive functioning in Alzheimer's disease (AD) across on year. Arch Gerontol Geriatr (2013) 56:96-103. doi:10.1016/j.archger.2012.06.016
11. Bowen ME. A prospective examination of the relationship between physical activity and dementia risk in later life. Am J Health Promot (2012) 26:333-40. doi:10.4278/ajhp.110311-QUAN-115
12. Middleton LE, Mitnitski A, Fallah N, Kirkland SA, Rockwood K. Changes in cognition and mortality in relation to exercise in late life: a population based study. PLoS One (2008) 3:e3124. doi:10.1371/journal.pone.0003124
13. Barnes D, Santos-Modesitt W, Poelke G, Kramer A, Castro C, Middelton L, et al. The mental activity and exercise (MAX) trial: a randomized controlled trial to enhance cognitive function in older adults. JAMA Intern Med (2013) 173:797-804. doi:10.1001/jamainternmed.2013.189
14. Chang S-H, Chen C-Y, Shen S-H, Chiou J-H. The effectiveness of an exercise programme for elders with dementia in a Taiwanese day-care centre. Int J Nurs Pract (2011) 17:213-20. doi:10.1111/j.1440-172X.2011.01928.x
15. Akishita M, Yamada S, Nishiya H, Sonohara K, Nakai R, Toba K. Effects of physical exercise on plasma concentrations of sex hormones in elderly women with dementia. J Am Geriatr Soc (2005) 53:1076-7. doi:10.1111/j.1532-5415.2005.53338_4.x
16. La Rue A, Felten K, Turkstra L. Intervention of multi-modal activities for older adults with dementia translation to rural communities. Am J Alzheimers Dis Other Demen (2015) 30:468-77. doi:10.1177/1533317514568888
17. Hagerman PA, Thomas VS. Gait performance in dementia: the effects of a 6-week resistance training program in an adult day-care setting. Int J Geriatr Psychiatry (2002) 17:329-34. doi:10.1002/gps.597
18. Uemura K, Shimada H, Makizako H, Doi T, Daisuke Y, Tsutsumimoto K, et al. Cognitive function affects trainability for physical performance in exercise intervention among older adults with mild cognitive impairment. Clin Interv Aging (2013) 8:97-102. doi:10.2147/CIA.S39434
19. Yu F, Leon AS, Bliss D, Dysken M, Savik K, Wyman JF. Aerobic training for older men with Alzheimer's disease: individual examples of progression. Res Gerontol Nurs (2011) 4:243-50. doi:10.3928/19404921-20110303-01
20. Ellis KA, Rainey-Smith SR, Rembach A, Macaulay SL, Villemagne VL. Enabling a multidisciplinary approach to the study of ageing and Alzheimer's disease: an update from the Australian Imaging Biomarkers and Lifestyle (AIBL) study. Int Rev Psychiatry (2013) 25:699-710. doi:10.3109/09540261.2013.870136
21. Brown BM, Peiffer JJ, Taddei K, Lui JK, Laws SM, Gupta VB, et al. Physical activity and amyloid- β plasma and brain levels: results from the Australian imaging, biomarkers and lifestyle study of ageing. Mol Psychiatry (2013) 18:875-81. doi:10.1038/mp.2012.107
22. Öhman H, Savikko N, Strandberg TE, Pitkälä KH. Effect of physical exercise on cognitive performance in older adults with mild cognitive impairment or dementia: a systematic review. Dement Geriatr Cogn Disord (2014) 38:347-65. doi:10.1159/000365388
23. Forbes D, Thiessen EJ, Blake CM, Forbes SC, Forbes S. Exercise programs for people with dementia. Cochrane Database Syst Rev (2013) 12:CD006489. doi:10.1002/14651858.CD006489.pub3
24. Kim B-K, Shin M-S, Kim C-J, Baek S-B, Ko Y-C, Kim Y-P. Treadmill exercise improves short-term memory by enhancing neurogenesis in amyloid beta-induced Alzheimer disease rats. J Exerc Rehabil (2014) 10:2-8. doi:10.12965/jer.140086
25. Adlard PA, Perreau VM, Pop V, Cotman CW. Voluntary exercise decreases amyloid load in a transgenic model of Alzheimer's disease. J Neurosci (2005) 25:4217-21. doi:10.1523/JNEUROSCI.0496-05.2005
26. Um H, Kang E, Leem Y, Cho I, Yang C, Chae K, et al. Exercise training acts as a therapeutic strategy for reduction of the pathogenic phenotypes for Alzheimer's disease in an NSE/APPsw-transgenic model. Int J Mol Med (2008) 4:529-39. doi:10.3892/ijmm
27. Marosi K, Bori Z, Hart N, Sárga L, Koltai E, Radák Z, et al. Long-term exercise treatment reduces oxidative stress in the hippocampus of aging rats. Neuroscience (2012) 226:21-8. doi:10.1016/j.neuroscience.2012.09.001
28. Okonkwo OC, Schultz SA, Oh JM, Larson J, Edwards D, Cook D, et al. Physical activity attenuates age-related biomarker alterations in preclinical AD. Neurology (2014) 83:1753-60. doi:10.1212/WNL.0000000000000964
29. Hamman RF, Wing RR, Edelstein SL, Lachin JM, Bray GA, Delahanty L, et al. Effect of weight loss with lifestyle intervention on risk of diabetes. Diabetes Care (2006) 26:2102-7. doi:10.2337/dc06-0560
30. Krause M, Rodrigues-Krause J, O'Hagan C, Medlow P, Davison G, Susta D, et al. The effects of aerobic exercise training at two different intensities in obesity and type 2 diabetes: implications for oxidative stress, low-grade inflammation and nitric oxide production. Eur J Appl Physiol (2014) 114:251-60. doi:10.1007/s00421-013-2769-6
31. Adamopoulos S, Schmid J-P, Dendale P, Poerschke D, Hansen D, Dritsas A, et al. Combined aerobic/inspiratory muscle training vs. aerobic training in patients with chronic heart failure: the Vent-HeFT trial: a European prospective multicentre randomized trial. Eur J Heart Fail (2014) 16:574-82. doi:10.1002/ejhf.70
32. Higgins JP, Green S. Cochrane Handbook for Systematic Review of Intervention. (2011).
33. Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group. Perferred reporting items for systematic reviews and meta-analysis: the PRISMA statement. PLoS Med (2009) 6. doi:10.1371/journal.pmed.1000097
34. Baker LD, Frank LL, Foster-Schubert K, Green PS, Wilkinson CW, McTiernan A, et al. Effects of aerobic exercise on mild cognitive impairment: a controlled trial. JAMA Neurol (2010) 67:71-9. doi:10.1001/archneurol.2009.307
35. Cheng S-T, Chow PK, Song Y-Q, Yu ECS, Chan ACM, Lee TMC, et al. Mental and physical activities delay cognitive decline in older persons with dementia. Am J Geriatr Psychiatry (2014) 22:63-74. doi:10.1016/j.jagp.2013.01.060
36. Coelho FG, de M, Andrade LP, Pedroso RV, Santos-Galduroz RF, Gobbi S, et al. Multimodal exercise intervention improves frontal cognitive functions and gait in Alzheimer's disease: a controlled trial. Geriatr Gerontol Int (2013) 13:198-203. doi:10.1111/j.1447-0594.2012.00887.x
37. Eggermont LHP, Swaab DF, Hol EM, Scherder EJ. Walking the line: a randomised trial on the effects of a short term walking programme on cognition in dementia. J Neurol Neurosurg Psychiatry (2009) 80:802-4. doi:10.1136/jnnp.2008.158444
38. Mancuso M, Filosto M, Bosetti F, Ceravolo R, Rocchi A, Tognoni G, et al. Decreased platelet cytochrome c oxidase activity is accompanied by increased blood lactate concentration during exercise in patients with Alzheimer disease. Exp Neurol (2003) 182:421-6. doi:10.1016/S0014-4886(03)00092-X
39. Nascimento CMC, Pereira JR, de Andrade LP, Garuffi M, Talib LL, Forlenza OV, et al. Physical exercise in MCI elderly promotes reduction of pro-inflammatory cytokines and improvements on cognition and BDNF peripheral levels. Curr Alzheimer Res (2014) 11:799-805. doi:10.2174/156720501108140910122849
40. Nascimento C, Pereira J, Pires de Andrade L, Garuffi M, Ayan C, et al. Physical exercise improves peripheral BDNF levels and cognitive fenctions in elderly mild cognitive impairment individuals with different BDNF Val166Met genotypes. J Alzheimers Dis (2015) 43(1):81-91. doi:10.3233/JAD-140576
41. Segal SK, Cotman CW, Cahill LF. Exercise-induced noradrenergic activation enhances memory consolidation in both normal aging and patients with amnestic mild cognitive impairment. J Alzheimers Dis (2012) 32:1011-8. doi:10.3233/JAD-2012-121078
42. Coelho FGDM, Vital TM, Stein AM, Arantes FJ, Rueda AV, Camarini R, et al. Acute aerobic exercise increases brain-derived neurotrophic factor levels in elderly with Alzheimer's disease. J Alzheimers Dis (2014) 39:401-8. doi:10.3233/JAD-131073
43. Lee C, Do Folsom AR, Blair SN. Physical activity and stroke risk: a meta-analysis. Stroke (2003) 34:2475-82. doi:10.1161/01.STR.0000091843.02517.9D
44. Ravona-Springer R, Lou X, Schmeidler J, Wysocki M, Lesser G, Rapp M, et al. Diabetes ia associated with increased rate of cognitive decline in questionably demented elderly. Dement Geriatr Cogn Disord (2010) 29:68-74. doi:10.1159/000265552
45. Ravona-Springer R, Moshier E, Schmeidler J, Godbold J, Akrivos J, Rapp M, et al. Changes in glycemic control are associated with chnages in cognition in non-diabetic alderly. J Alzheimers Dis (2012) 30:299-309. doi:10.3233/JAD-2012-120106.Changes
46. Casley CS, Canevari L, Land JM, Clark JB, Sharpe MA. Beta-amyloid inhibits integrated mitochondrial respiration and key enzyme activities. J Neurochem (2002) 80:91-100. doi:10.1046/j.0022-3042.2001.00681.x
47. Raha S, Robinson BH. Mitochondria, oxygen free radicals, and apoptosis. Am J Med Genet (2001) 106:62-70. doi:10.1002/ajmg.1398
48. Amor S, Puentes F, Baker D, van der Valk P. Inflammation in neurodegenerative diseases. Immunology (2010) 129:154-69. doi:10.1111/j.1365-2567.2009.03225.x
49. Faria MC, Gonçalves GS, Rocha NP, Moraes EN, Bicalho MA, Gualberto Cintra MT, et al. Increased plasma levels of BDNF and inflammatory markers in Alzheimer's disease. J Psychiatr Res (2014) 53:166-72. doi:10.1016/j.jpsychires.2014.01.019
50. McGeer EG, McGeer PL. Neuroinflammation in Alzheimer's disease and mild cognitive impairment: a field in its infancy. J Alzheimers Dis (2010) 19:355-61. doi:10.3233/JAD-2010-1219
51. Brosseron F, Krauthausen M, Kummer M, Heneka MT. Body fluid cytokine levels in mild cognitive impairment and Alzheimer's disease: a comparative overview. Mol Neurobiol (2014) 50:534-44. doi:10.1007/s12035-014-8657-1
52. Souza LC, Filho CB, Goes ATR, Fabbro L, Del, de Gomes MG, Savegnago L, et al. Neuroprotective effect of physical exercise in a mouse model of Alzheimer's disease induced by β-amyloid1-40 peptide. Neurotox Res (2013) 24:148-63. doi:10.1007/s12640-012-9373-0
53. Erickson K, Miller D, Roecklein K. The aging hippocampus:interactions between exercise, depression, and BDNF. Neuroscientist (2012) 18:82-97. doi:10.1177/1073858410397054.The
54. Phung TK, Waltroft BL, Laursen TM, Settnes A, Kessing LV, Mortensen PB, et al. Hysterectomy, oophorectomy and risk of dementia: a nationwide historical cohort study. Dement Geriatr Cogn Disord (2010) 30:43-50. doi:10.1159/000314681
55. Jurkowki JE, Jones NL, Ealker C, Younglai EV, Sutton JR. Ovarian hormonal responses to exercise. J Appl Physiol Respir Env Exerc Physiol (1978) 44:109-14.
56. Bonen A, Ling W, MacIntyre K, Neil R, McGrail J, Belcastro A. Effects of exericse on the serum concentration of FSH, LH, progesterone, and esterdiol. Eur J Appl Physiol Occup Physiol (1979) 42:15-23. doi:10.1007/BF00421100
57. Zmuda JM, Thompson PD, Winthers SJ. Exercise increases serum testosterone and sex hormone-binding globulin levels in older men. Metabolism (1996) 45:935-9. doi:10.1016/S0026-0495(96)90258-9
58. Segal SK, Cahill L. Endogenous noradrenergic activation and memory for emotional material in men and women. Psychoneuroendocrinology (2009) 34:1263-71. doi:10.1016/j.psyneuen.2009.04.020
59. McIntyre CK, Hatfield T, McGaugh JL. Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats. Eur J Neurosci (2002) 16:1223-6. doi:10.1046/j.1460-9568.2002.02188.x
60. Galvez R, Mesches MH, McGaugh JL. Norepinephrine release in the amygdala in response to footshock stimulation. Neurobiol Learn Mem (1996) 66:253-7. doi:10.1006/nlme.1996.0067
61. Baker LD, Bayer-Carter JL, Skinner J, Montine TJ, Cholerton BA, Callaghan M, et al. High-intensity physical activity modulates diet effects on cerebrospinal amyloid- β levels in normal aging and mild cognitive impairment. J Alzheimers Dis (2012) 28:137-46. doi:10.3233/JAD-2011-111076
62. Maesako M, Uemura K, Kubota M, Sasaki H, Hayashida N, Asada-Utsugi M, et al. Exercise is more effective than diet control in preventing high fat diet-induced beta-amyloid deposition and memory deficit in amyloid precursor protein transgenic mice. J Biol (2012) 287:23024-33. doi:10.1074/jbc.M112.367011
63. Lin X, Zhang X, Guo J, Roberts C, McKenzie S, Wu W, et al. Effects of exercise training on cardiorespiratory fitness and biomarkers of cardimetabolic health: a systematic review and meta-analysis of randomized controlled trials. J Am Hear Assoc (2015) 4(7). doi:10.1161/JAHA.115.002014
64. Brüünsgaard H, Pedersen B. Age-related inflammatory cytokines and disease. Immunol Allergy Clin North Am (2003) 23:15-39. doi:10.1016/S0889-8561(02)00056-5
65. Woods JA, Wilund KR, Martin SA, Kistler BM. Exercise, inflammation and aging. Aging Dis (2012) 3:130-40.
66. Yeh S, Lin L, Chuang Y, Liu C, Tsai F, Lee M, et al. Effects of music aerobic exercise on depression and brain-derived neurotrophic factor levels in community dwelling women. Biomed Res Int (2015) 2015:135893. doi:10.1155/2015/135893
67. Erickson KI, Prakash RS, Voss MW, Chaddock L, Heo S, McLaren M, et al. Brain-derived neurotrophic factor is associated with age-related decline in hippocampal volume. J Neurosci (2010) 30:5368-75. doi:10.1523/JNEUROSCI.6251-09.2010
68. Hauser PS, Ryan RO. Impact of Apolipoprotein E on Alzheimer's disease. Curr Alzheimer Res (2013) 10:809-17. doi:10.2174/15672050113109990156
69. Nichol K, Deeny SP, Seif J, Camaclang K, Cotman CW. Exercise improves cognition and hippocampal plasticity in APOE e4 mice. Alzheimers Dement (2009) 5:287-94. doi:10.1016/j.jalz.2009.02.006
70. Rasmussen KL, Tybjaerg-Hansen A, Nordestgaard BG, Frikke-Schmidt R. Plasma levels of apolipoprotein E and risk of dementia in the general population. Ann Neurol (2015) 77:301-11. doi:10.1002/ana.24326
71. Hohman TJ, Bell SP, Jefferson AL. The role of vascular endothelial growth factor in neurodegeneration and cognitive decline: exploring interactions with biomarkers of Alzheimer disease. JAMA Neurol (2015) 72:520-9. doi:10.1001/jamaneurol.2014.4761
72. Petersen AMW, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol (2005) 98:1154-62. doi:10.1152/japplphysiol.00164.2004
73. Holtzman D. CSF biomarkers for Alzheimer's disease: current utility and potential future use. Neurobiol Aging (2011) 32(Suppl 1):9. doi:10.1016/j.neurobiolaging.2011.09.003
74. Andreasen N, Minthon L, Davidsson P, Vanmechelen E, Vanderstichele H, Winblad B, et al. Evaluation of CSF-tau and CSF-amyloid beta42 as diagnostic markers for Alzheimer disease in clinical practice. Arch Neurol (2001) 58:373-9. doi:10.1001/archneur.58.3.373
75. Gao L, Tang H, Nie K, Wnag L, Zhao J, Gan R, et al. Cerebrospinal fluid alpha-synuclein as a bioamrkers for Parkinson's disease diagnosis: a systematic review and meta-analysis. Int J Neurosci (2014) 125(9):645-54. doi:10.3109/00207454.2014.961454
76. Wild E, Robertson N, Miller J, Traeger U, Haider S, Mcdonalds D, et al. Quantifying mutant huntingtin in Huntington's disease CSF. J Neurol Neurosurg Psychiatry (2014) 85. doi:10.1136/jnnp-2014-309236.23
77. del Campo M, Mollenhauer B, Bertolotto A, Engelborghs S, Hampel H, Simonsen AH, et al. Recommendations to standardize preanalytical confounding factors in Alzheimer's and Parkinson's disease cerebrospinal fluid biomarkers: an update. Biomark Med (2012) 6:419-30. doi:10.2217/bmm.12.46
78. Hoffmann K, Frederiksen KS, Sobol NA, Beyer N, Vogel A, Simonsen AH, et al. Preserving cognition, quality of life, physical health and functional ability in Alzheimer's disease: the effect of physical exercise (ADEX trial): rationale and design. Neuroepidemiology (2013) 41:198-207. doi:10.1159/000354632