Distinctive Effects of Aerobic and Resistance Exercise Modes on Neurocognitive and Biochemical Changes in Individuals with Mild Cognitive Impairment

Author(s): Chia-Liang Tsai*, Ming-Chyi Pai, Jozef Ukropec, Barbara Ukropcová*.

Journal Name: Current Alzheimer Research

Volume 16 , Issue 4 , 2019

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Abstract:

Background: Decreased levels of the neuroprotective growth factors, low-grade inflammation, and reduced neurocognitive functions during aging are associated with neurodegenerative diseases, such as Alzheimer’s disease. Physical exercise modifies these disadvantageous phenomena while a sedentary lifestyle promotes them.

Purpose: The purposes of the present study included investigating whether both aerobic and resistance exercise produce divergent effects on the neuroprotective growth factors, inflammatory cytokines, and neurocognitive performance, and further exploring whether changes in the levels of these molecular biomarkers are associated with alterations in neurocognitive performance.

Methods: Fifty-five older adults with amnestic MCI (aMCI) were recruited and randomly assigned to an aerobic exercise (AE) group, a resistance exercise (RE) group, or a control group. The assessment included neurocognitive measures [e.g., behavior and event-related potential (ERP)] during a task-switching paradigm, as well as circulating neuroprotective growth factors (e.g., BDNF, IGF-1, VEGF, and FGF-2) and inflammatory cytokine (e.g., TNF-α, IL-1β, IL-6, IL-8, and IL-15) levels at baseline and after either a 16-week aerobic or resistance exercise intervention program or a control period.

Results: Aerobic and resistance exercise could effectively partially facilitate neurocognitive performance [e.g., accuracy rates (ARs), reaction times during the heterogeneous condition, global switching cost, and ERP P3 amplitude] when the participants performed the task switching paradigm although the ERP P2 components and P3 latency could not be changed. In terms of the circulating molecular biomarkers, the 16-week exercise interventions did not change some parameters (e.g., leptin, VEGF, FGF-2, IL-1β, IL-6, and IL-8). However, the peripheral serum BDNF level was significantly increased, and the levels of insulin, TNF-α, and IL-15 levels were significantly decreased in the AE group, whereas the RE group showed significantly increased IGF-1 levels and decreased IL-15 levels. The relationships between the changes in neurocognitive performance (AR and P3 amplitudes) and the changes in the levels of neurotrophins (BDNF and IGF-1)/inflammatory cytokines (TNF-α) only approached significance.

Conclusion: These findings suggested that in older adults with aMCI, not only aerobic but also resistance exercise is effective with regard to increasing neurotrophins, reducing some inflammatory cytokines, and facilitating neurocognitive performance. However, the aerobic and resistance exercise modes likely employed divergent molecular mechanisms on neurocognitive facilitation.

Keywords: Aerobic exercise, resistance exercise, cognition, molecular mediators of exercise-induced response, mild cognitive impairment, Alzheimer's disease.

[1]
Laske C, Stellos K, Hoffmann N, Stransky E, Straten G, Eschweiler GW, et al. Higher BDNF serum levels predict slower cognitive decline in Alzheimer’s disease patients. Int J Neuropsychopharmacol 14: 399-04. (2011).
[2]
Yasutake C, Kuroda K, Yanagawa T, Okamura T, Yoneda H. Serum BDNF, TNF-alpha and IL-1beta levels in dementia patients: comparison between Alzheimer’s disease and vascular dementia. Eur Arch Psychiatry Clin Neurosci 256: 402-6. (2006).
[3]
Yu H, Zhang Z, Shi Y, Bai F, Xie C, Qian Y, et al. Association study of the decreased serum BDNF concentrations in amnestic mild cognitive impairment and theVal66Met polymorphism in Chinese Han J. Clin Psychiatry 69: 1104-11. (2008).
[4]
Murialdo G, Barreca A, Nobili F, Rollero A, Timossi G, Gianelli MV, et al. Relationships between cortisol, dehydroepiandrosteronesulphate and insulin-like growth factor-I system in dementia. J Endocrinol Invest 24: 139-46. (2001).
[5]
Solerte SB, Ferrari E, Cuzzoni G, Locatelli E, Giustina A, Zamboni M, et al. Decreased release of the angiogenic peptide vascular endothelial growth factor in Alzheimer’s disease: recovering effect with insulin and DHEA sulfate. Dement Geriatr Cogn Disord 19: 1-10. (2005).
[6]
Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci USA 100: 14385-90. (2003).
[7]
Shetty AK, Hattiangady B, Shetty GA. Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: role of astrocytes. Glia 51: 173-86. (2005).
[8]
Connor B, Young D, Yan Q, Faull RL, Synek B, Dragunow M. Brain-derived neurotrophic factor is reduced in Alzheimer’s disease. Brain Res Mol Brain Res 49: 71-81. (1997).
[9]
Garzon D, Yu G, Fahnestock M. A new brain-derived neurotrophic factor transcript and decrease in brain-derived neurotrophic factor transcripts 1, 2 and 3 in Alzheimer’s disease parietal cortex. J Neurochem 82: 1058-64. (2002).
[10]
Holsinger RM, Schnarr J, Henry P, Castelo VT, Fahnestock M. Quantitation of BDNF mRNA in human parietal cortex by competitive reverse transcription-polymerase chain reaction: Decreased levels in Alzheimer’s disease. Brain Res Mol Brain Res 76: 347-54. (2000).
[11]
Gezen-Ak D, Dursun E, Hanağası H, Bilgiç B, Lohman E, Araz ÖS, et al. BDNF, TNFα, HSP90, CFH, and IL-10 serum levels in patients with early or late onset Alzheimer’s disease or mild cognitive impairment. J Alzheimers Dis 37: 185-95. (2013).
[12]
Peng S, Wuu J, Mufson EJ, Fahnestock M. Precursor form of brain-derived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre-clinical stages of Alzheimer’s disease. J Neurochem 93: 1412-21. (2005).
[13]
Shimada H, Makizako H, Doi T, Yoshida D, Tsutsumimoto K, Anan Y, et al. A large, cross-sectional observational study of serum BDNF, cognitive function, and mild cognitive impairment in the elderly. Front Aging Neurosci 6: 69. (2014).
[14]
Carro E, Trejo JL, Gomez-Isla T, LeRoith D, Torres-Aleman I. Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nat Med 8: 1390-7. (2002).
[15]
Arvat E, Broglio F, Ghigo E. Insulin-Like growth factor I: implications in aging. Drugs Aging 16: 29-40. (2000).
[16]
Vagnucci AHJr. Li WW. Alzheimer’s disease and angiogenesis. Lancet 361: 605-8. (2003).
[17]
DeCarli C, Mungas D, Harvey D, et al. Memory impairment, but not cerebrovascular disease, predicts progression of MCI to dementia. Neurology 63: 220-7. (2004).
[18]
Wilson CJ, Finch CE, Cohen HJ. Cytokines and cognition-the case for a head-to-toe inflammatory paradigm. J Am Geriatr Soc 50: 2041-56. (2002).
[19]
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 50: 534-44. (2014).
[20]
Diniz BS, Teixeira AL, Ojopi EB, Talib LL, Mendonça VA, Gattaz WF, et al. Higher serum sTNFR1 level predicts conversion from mild cognitive impairment to Alzheimer’s disease. J Alzheimers Dis 22: 1305-11. (2010).
[21]
McGeer EG, McGeer PL. Neuroinflammation in Alzheimer’s disease and mild cognitive impairment: a field in its infancy. J Alzheimers Dis 19: 355-61. (2010).
[22]
Galimberti D, Schoonenboom N, Scheltens P, Fenoglio C, Bouwman F, Venturelli E, et al. Intrathecal chemokine synthesis in mild cognitive impairment and Alzheimer disease. Arch Neurol 63: 538-43. (2006).
[23]
Angelopoulos P, Agouridaki H, Vaiopoulos H, Siskou E, Doutsou K, Costa V, et al. Cytokines in Alzheimer’s disease and vascular dementia. Int J Neurosci 118: 1659-72. (2008).
[24]
Angelopoulos P, Agouridaki H, Vaiopoulos H, Siskou E, Doutsou K, Costa V, et al. Cytokines in Alzheimer’s disease and vascular dementia. Int J Neurosci 118: 1659-72. (2008).
[25]
Cojocaru IM, Cojocaru M, Miu G, Sapira V. Study of interleukin-6 production in Alzheimer’s disease. Rom J Intern Med 49: 55-58 (2011).
[26]
Forlenza OV, Diniz BS, Talib LL, Mendonca VA, Ojopi EB, Gattaz WF, et al. Increased serum IL-1beta level in Alzheimer’s disease and mild cognitive impairment. Dement Geriatr Cogn Disord 28: 507-12. (2009).
[27]
Guerreiro RJ, Santana I, Bras JM, Santiago B, Paiva A, Oliveira C. Peripheral inflammatory cytokines as biomarkers in Alzheimer’s disease and mild cognitive impairment. Neurodegener Dis 4: 406-12. (2007).
[28]
Magaki S, Mueller C, Dickson C, Kirsch W. Increased production of inflammatory cytokines in mild cognitive impairment. Exp Gerontol 42: 233-40. (2007).
[29]
Rentzos M, Zoga M, Paraskevas GP, Kapaki E, Rombos A, Nikolaou C, et al. IL-15 is elevated in cerebrospinal fluid of patients with Alzheimer’s disease and frontotemporal dementia. J Geriatr Psychiatry Neurol 19: 114-7. (2006).
[30]
Lombardi VR, Garcia M, Rey L, Cacabelos R. Characterization of cytokine production, screening of lymphocyte subset patterns and in vitro apoptosis in healthy and Alzheimer’s disease (AD) individuals. J Neuroimmunol 97: 163-71. (1999).
[31]
Alvarez A, Cacabelos R, Sanpedro C, Garcia-Fantini M, Aleixandre M. Serum TNF-α levels are increased and correlate negatively with free IGF-I in Alzheimer disease. Neurobiol Aging 28: 533-6. (2007).
[32]
Bermejo P, Martin-Aragon S, Benedi J, Susin C, Felici E, Gil P, et al. Differences of peripheral inflammatory markers between mild cognitive impairment and Alzheimer’s disease. Immunol Lett 117: 198-02. (2008).
[33]
Bruunsgaard H, Pedersen M, Pedersen BK. Aging and proinflammatory cytokines. Curr Opin Hematol 8: 131-6. (2001).
[34]
Pratico D, Trojanowski JQ. Inflammatory hypotheses: novel mechanisms of Alzheimer’s neurodegeneration and new therapeutic targets? Neurobiol Aging 21: 441-5. (2000).
[35]
Morgan AR, Touchard S, O’Hagan C, Sims R, Majounie E, Escott-Price V, et al. The correlation between inflammatory biomarkers and polygenic risk score in alzheimer’s disease. J Alzheimers Dis 56: 25-36. (2017).
[36]
Flex A, Giovannini S, Biscetti F, Liperoti R, Spalletta G, Straface G, et al. Effect of proinflammatory gene polymorphisms on the risk of Alzheimer’s disease. Neurodegener Dis 13: 230-6. (2014).
[37]
Naj AC, Jun G, Reitz C, Kunkle BW, Perry W, Park YS, et al. Effects of multiple genetic loci on age at onset in late-onset Alzheimer disease: a genome-wide association study. JAMA Neurol 71: 1394-404. (2014).
[38]
Guerreiro R, Wojtas A, Bras J, Carrasquillo M, Rogaeva E, Majounie E, et al. TREM2 variants in Alzheimer’s disease. N Engl J Med 368: 117-27. (2013).
[39]
Pedersen BK. The diseasome of physical inactivity-and the role of myokines in muscle-fat cross talk. J Physiol 587: 5559-68. (2009).
[40]
Liang KY, Mintun MA, Fagan AM, Goate AM, Bugg JM, Holtzman DM, et al. Exercise and Alzheimer’s disease biomarkers in cognitively normal older adults. Ann Neurol 68: 311-8. (2010).
[41]
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. Arch Neurol 67: 71-9. (2010).
[42]
Kwak YS, Um SY, Son TG, Kim DJ. Effect of regular exercise on senile dementia patients. Int J Sports Med 29: 471-4. (2008).
[43]
Tsai CL, Pan CY, Chen FC, Tseng YT. Open- and closed-skill exercise interventions produce different neurocognitive effects on executive functions in the elderly: a 6-month randomized, controlled trial. Front Aging Neurosci 9: 294. (2017).
[44]
Carson BP. The potential role of contraction-induced myokines in the regulation of metabolic function for the prevention and treatment of Type 2 diabetes. Front Endocrinol 8: 97. (2017).
[45]
Cassilhas RC, Viana VA, Grassmann V, Santos RT, Santos RF, Tufik S, et al. The impact of resistance exercise on the cognitive function of the elderly. Med Sci Sports Exerc 39: 1401-7. (2007).
[46]
Gomez-Pinilla F, Dao L, So V. Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res 764: 1-8. (1997).
[47]
Gómez-Pinilla F, So V, Kesslak JP. Spatial learning and physical activity contribute to the induction of fibroblast growth factor: neural substrates for increased cognition associated with exercise. Neuroscience 85: 53-61. (1998).
[48]
Maass A, Düzel S, Brigadski T, Goerke M, Becke A, Sobieray U, et al. Relationships of peripheral IGF-1, VEGF and BDNF levels to exercise-related changes in memory, hippocampal perfusion and volumes in older adults. Neuroimage 131: 142-54. (2016).
[49]
Ruscheweyh R, Willemer C, Kruger K, Duning T, Warnecke T, Sommer J, et al. Physical activity and memory functions: an interventional study. Neurobiol Aging 32: 1304-19. (2011).
[50]
Tsai CL, Wang CH, Pan CY, Chen FC, Huang TH. The effect of long-term resistance exercise on the relationship between neurotrophin levels and cognitive performance in the elderly. Front Behav Neurosci 9: 23. (2015).
[51]
Tsai CL, Ukropec J, Ukropcová B, Pai MC. An acute bout of aerobic or strength exercise specifically modifies circulating exerkine levels and neurocognitive functions in elderly individuals with mild cognitive impairment. Neuroimage Clin 17: 272-84. (2018).
[52]
Voss MW, Erickson KI, Prakash RS, Chaddock L, Kim EL, Alves H, et al. Neurobiological markers of exercise-related brain plasticity in older adults. Brain Behav Immun 28: 90-9. (2013).
[53]
Zoladz JA, Pilc A, Majerczak J, Grandys M, Zapart-Bukowska J, Duda K. Endurance training increases plasma brain derived neurotrophic factor concentration in young healthy men. J Physiol Pharmacol 59: 119-32. (2008).
[54]
Elosua R, Bartali B, Ordovas JM, Corsi AM, Lauretani F, Ferrucci L. Association between physical activity, physical performance, and inflammatory biomarkers in an elderly population: the InCHIANTI study. J Gerontol A Biol Sci Med Sci 60: 760-7. (2005).
[55]
Nascimento CM, 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 11: 799-805. (2014).
[56]
Nielsen AR, Pedersen BK. The biological roles of exercise-induced cytokines: IL-6, IL-8, and IL-15. Appl Physiol Nutr Metab 32: 833-9. (2007).
[57]
Cotman CW, Berchtold NC, Christie LA. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30: 464-72. (2007).
[58]
Stranahan AM, Martin B, Maudsley S. Anti-inflammatory effects of physical activity in relationship to improved cognitive status in humans and mouse models of Alzheimer’s disease. Curr Alzheimer Res 9: 86-92. (2012).
[59]
Cassilhas RC, Lee KS, Fernandes J, Oliveira MG, Tufik S, Meeusen R, et al. Spatial memory is improved by aerobic and resistance exercise through divergent molecular mechanisms. Neuroscience 202: 309-17. (2012).
[60]
Liu-Ambrose T, Nagamatsu LS, Graf P, Beattie BL, Ashe MC, Handy TC. Resistance training and executive functions: a 12-month randomized controlled trial. Arch Intern Med 170: 170-8. (2010).
[61]
Perrig-Chiello P, Perrig WJ, Ehrsam R, Staehelin HB, Krings F. The effects of resistance training on well-being and memory in elderly volunteers. Age Ageing 27: 469-75. (1998).
[62]
Tsai CL, Wang WL. Exercise-mode-related changes in task-switching performance in the elderly. Front Behav Neurosci 9: 56. (2015).
[63]
ten Brinke LF, Bolandzadeh N, Nagamatsu LS, Hsu CL, Davis JC, Miran-Khan K, et al. Aerobic exercise increases hippocampal volume in older women with probable mild cognitive impairment: a 6-month randomised controlled trial. Br J Sports Med 49: 248-54. (2015).
[64]
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 86: 876-84. (2011).
[65]
Portugal EM, Vasconcelos PG, Souza R, Lattari E, Monteiro-Junior RS, Machado S, et al. Aging process, cognitive decline and Alzheimer’s disease: can strength training modulate these responses? CNS Neurol Disord Drug Targets 14: 1209-13. (2015).
[66]
Espinosa A, Alegret M, Valero S, Vinyes-Junque G, Hernandez I, Mauleon A, et al. A longitudinal follow-up of 550 mild cognitive impairment patients: evidence for large conversion to dementia rates and detection of major risk factors involved. J Alzheimers Dis 34: 769-80. (2013).
[67]
Morris JC, Storandt M, Miller P, McKeel Jr DW, Price JL, Rubin EH, et al. Mild cognitive impairment represents early-stage Alzheimer’s disease. Arch Neurol 58: 397-405. (2001).
[68]
Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E. Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 56: 303-8. (1999).
[69]
Amieva H, Letenneur L, Dartigues JF, Rouch-Leroyer I, Sourgen C, D’Alchée-Birée F, et al. Annual rate and predictors of conversion to dementia in subjects presenting mild cognitive impairment criteria defined according to a population-based study. Dement Geriatr Cogn Disord 18: 87-93. (2004).
[70]
Fisk JD, Merry HR, Rockwood K. Variations in case definition affect prevalence but not outcomes of mild cognitive impairment. Neurology 61: 1179-84. (2003).
[71]
Belleville S, Bherer L, Lepage E, Chertkow H, Gauthier S. Task switching capacities in persons with Alzheimer’s disease and mild cognitive impairment. Neuropsychologia 46: 2225-33. (2008).
[72]
Tsai CL, Pai MC, Ukropec J, Ukropcová B. The role of physical fitness in the neurocognitive performance of task switching in older persons with mild cognitive impairment. J Alzheimers Dis 53: 143-59. (2016).
[73]
Guiney H, Machado L. Benefits of regular aerobic exercise for executive functioning in healthy populations. Psychon Bull Rev 20: 73-86. (2013).
[74]
Hillman CH, Kramer AF, Belopolsky AV, Smith DP. A cross-sectional examination of age and physical activity on performance and event-related brain potentials in a task switching paradigm. Int J Psychophysiol 59: 30-9. (2006).
[75]
Suzuki T, Shimada H, Makizako H, Doi T, Yoshida D, Tsutsumimoto K, et al. Effects of multicomponent exercise on cognitive function in older adults with amnestic mild cognitive impairment: a randomized controlled trial. BMC Neurol 12: 128. (2012).
[76]
Suzuki T, Shimada H, Makizako H, Doi T, Yoshida D, Ito K, et al. A randomized controlled trial of multicomponent exercise in older adults with mild cognitive impairment. PLoS One 8: e61483. (2013).
[77]
Gauthier S, Reisberg B, Zaudig M, Petersen RC, Ritchie K, Broich K, et al. Mild cognitive impairment. Lancet 367: 1262-70. (2006).
[78]
Petersen RC. Mild cognitive impairment as a diagnostic entity. J Intern Med 256: 183-94. (2004).
[79]
Winblad B, Palmer K, Kivipelto M, Jelic V, Fratiglioni L, Wahlund LO, et al. Mild cognitive impairment - beyond controversies, towards a consensus: report of the international working group on mild cognitive impairment. J Intern Med 256: 240-6. (2004).
[80]
Teng EL, Hasegawa K, Homma A, Imai Y, Larson E, Graves A, et al. The Cognitive Abilities Screening Instrument (CASI): a practical test for cross-cultural epidemiological studies of dementia. Int Psychogeriatr 6: 45-58. (1994).
[81]
Beck AT, Steer RA, Brown GK. BDI-II: 2nd edition manual. The Psychological Corporation, San Antonio, T.X. (1996)
[82]
Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9: 97-13. (1971).
[83]
Wu PW. A study of the relationships among interpersonal intimacy, social participation, and mental health in elders. Unpublished master’s dissertation, National Taipei University of Education, Taipei (2011)
[84]
Wechsler D. Wechsler Adult Intelligence Scale-Fourth Edition (WAIS-IV) Technical and Interpretive Manual. San Antonio, Texas: Pearson (2008).
[85]
Thomas S, Reading J, Shephard RJ. Revision of the physical activity readiness questionnaire (PAR-Q). Can J Sport Sci 17: 3338-45. (1992).
[86]
Sallis JF, Haskell WL. Physical activity assessment methodology in the five-city project. Am J Epidemiol 121: 91-106. (1985).
[87]
Rikli RE, Jones CJ. Senior Fitness Test Manual (2nd ed.). United States: Human Kinetics (2012).
[88]
Kline GM, Porcari JP, Hintermeister R, Freedson PS, Ward A, McCarron RF, et al. Estimation of VO2max from a one-mile track walk, gender, age, and body weight. Med Sci Sports Exerc 19: 253-9. (1987).
[89]
McAuley E, Szabo AN, Mailey EL, Erickson KI, Voss M, White SM, et al. Non-exercise estimated cardiorespiratory fitness: Associations with brain structure, cognition, and memory complaints in older adults. Ment Health Phys Act 4: 5-11. (2011).
[90]
Amarante do Nascimento M, Januário RS, Gerage AM, Mayhew JL, Cheche Pina FL, et al. Familiarization and reliability of one repetition maximum strength testing in older women. J Strength Cond Res 27: 1636-42. (2013).
[91]
Dixit A, Vaney N, Tandon OP. Evaluation of cognitive brain functions in caffeine users: a P3 evoked potential study. Indian J Physiol Pharmacol 50: 175-80. (2006).
[92]
Geisler MW, Polich J. P300 and time of day: circadian rhythms, food intake, and body temperature. Biol Psychol 31: 117-36. (1990).
[93]
Wu BH. Dose effects of caffeine ingestion on acute hormonal responses to resistance exercise. J Sports Med Phys Fitness 55: 1242-51. (2014).
[94]
Nascimento CM, Pereira JR, Pires de Andrade L, Garuffi M, Ayan C, Kerr DS, et al. Physical exercise improves peripheral BDNF levels and cognitive functions in mild cognitive impairment elderly with different bdnf Val66Met genotypes. J Alzheimers Dis 43: 81-91. (2015).
[95]
Boot WR, Simons DJ, Stothart C, Stutts C. The pervasive problem with placebos in psychology: why active control groups are not sufficient to rule out placebo effects. Perspect Psychol Sci 8: 445-54. (2013).
[96]
Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA 108: 3017-22. (2011).
[97]
Zheng G, Xia R, Zhou W, Tao J, Chen L. Aerobic exercise ameliorates cognitive function in older adults with mild cognitive impairment: a systematic review and meta-analysis of randomised controlled trials. Br J Sports Med 50: 1443-50. (2016).
[98]
Cohen J. Eta-squared and partial eta-squared in fixed factor ANOVA designs. Educ Psychol Meas 33: 107-12. (1973).
[99]
O’Connell RG, Balsters JH, Kilcullen SM, Campbell W, Bokde AW, Lai R, et al. A simultaneous ERP/fMRI investigation of the P300 aging effect. Neurobiol Aging 33: 2448-61. (2012).
[100]
Missonnier P, Deiber MP, Gold G, Herrmann FR, Millet P, Michon A, et al. Working memory load-related electroencephalographic parameters can differentiate progressive from stable mild cognitive impairment. Neuroscience 150: 346-56. (2007).
[101]
Jiang S, Qu C, Wang F, Liu Y, Qiao Z, Qiu X, et al. Using event-related potential P300 as an electrophysiological marker for differential diagnosis and to predict the progression of mild cognitive impairment: A meta-analysis. Neurol Sci 36: 1105-12. (2015).
[102]
Friedman D, Nessler D, Johnson R Jr, Ritter W, Bersick M. Age-related changes in executive function: an event-related potential (ERP) investigation of task-switching. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 15: 95-128. (2008).
[103]
van Praag H, Christie BR, Sejnowski TJ, Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96: 13427-31. (1999).
[104]
Tapia-Arancibia L, Aliaga E, Silhol M, Arancibia S. New insights into brain BDNF function in normal aging and Alzheimer disease. Brain Res Rev 59: 201-20. (2008).
[105]
Ye X, Tai W, Zhang D. The early events of Alzheimer’s disease pathology: From mitochondrial dysfunction to BDNF axonal transport deficits. Neurobiol Aging 33: 1122 e1-10 (2012).
[106]
Phillips HS, Hains JM, Armanini M, Laramee GR, Johnson SA, Winslow JW. BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer’s disease. Neuron 7: 695-702. (1991).
[107]
Gomes da Silva S, Unsain N, Mascó DH, Toscano-Silva M, de Amorim HA, Silva Araújo BH, et al. Early exercise promotes positive hippocampal plasticity and improves spatial memory in the adult life of rats. Hippocampus 22: 347-58. (2012).
[108]
Pan W, Banks WA, Fasold MB, Bluth J, Kastin AJ. Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology 37: 1553-61. (1998).
[109]
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 110: 285-93. (2010).
[110]
Rojas V, Knicker A, Hollmann W, Bloch W, Struder HK. Effect of resistance exercise on serum levels of growth factors in humans. Horm Metab Res 42: 982-6. (2010).
[111]
Lichtenwalner RJ, Forbes ME, Bennett SA, Lynch CD, Sonntag WE, Riddle DR. Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience 107: 603. (2001).
[112]
Niikura T, Hashimoto Y, Okamoto T, Abe Y, Yasukawa T, Kawasumi M, et al. Insulin-like growth factor I (IGF-I) protects cells from apoptosis by Alzheimer’s V642I mutant amyloid precursor protein through IGF-I receptor in an IGF-binding protein-sensitive manner. J Neurosci 21: 1902-10. (2001).
[113]
Schiffer T, Schulte S, Hollmann W, Bloch W, Struder HK. Effects of strength and endurance training on brain-derived neurotrophic factor and insulin-like growth factor 1 in humans. Horm Metab Res 41: 250-4. (2009).
[114]
Arikawa AY, Kurzer MS, Thomas W, Schmitz KH. No effect of exercise on insulin-like growth factor-I, insulin, and glucose in young women participating in a 16-week randomized controlled trial. Cancer Epidemiol Biomarkers Prev 19: 2987-90. (2010).
[115]
Borst SE, De Hoyos DV, Garzarella L, Vincent K, Pollock BH, Lowenthal DT, et al. Effects of resistance training on insulin-like growth factor-I and IGF binding proteins. Med Sci Sports Exerc 33: 648-53. (2001).
[116]
Ding Y, Li J, Zhou Y, Rafols JA, Clark JC, Ding Y. Cerebral angiogenesis and expression of angiogenic factors in aging rats after exercise. Curr Neurovasc Res 3: 15-23. (2006).
[117]
Park J, Nakamura Y, Kwon Y, Park H, Kim E, Park S. The effect of combined exercise training on carotid artery structure and function, and vascular endothelial growth factor (VEGF) in obese older women. Jan J Phys Fitness Sports Med 59: 495-504. (2010).
[118]
Sandri M, Adams V, Gielen S, Linke A, Lenk K, Krankel N, et al. Effects of exercise and ischemia on mobilization and functional activation of blood-derived progenitor cells in patients with ischemic syndromes: Results of 3 randomized studies. Circulation 111: 3391-9. (2005).
[119]
Beck EB, Erbs S, Mobius-Winkle S, Adams V, Woitek FJ, Walther T, et al. Exercise training restores the endothelial response to vascular growth factors in patients with stable coronary artery disease. Eur J Prev Cardiol 19: 412-8. (2012).
[120]
Schalager O, Giurgea A, Schuhfried O, Seidinger D, Hammer A, Groger M, et al. Exercise training increases endothelial progenitor cells and decreases asymmetric dimethylarginine in peripheral arterial disease: a randomized controlled trial. Atherosclerosis 217: 240-8. (2011).
[121]
Ogawa K, Sanada K, Machida S, Okutsu M, Suzuki K. Resistance exercise training-induced muscle hypertrophy was associated with reduction of inflammatory markers in elderly women. Mediators Inflamm 2010: 20171023. (2010).
[122]
Dickstein JB, Moldofsky H, Hay JB. Brain-blood permeability: TNF-α promotes escape of protein tracer from CSF to blood. Am J Physiol Regul Integr Comp Physiol 279: R148-51. (2000).
[123]
Venters HD, Tang Q, Liu Q, VanHoy RW, Dantzer R, Kelley KW. A new mechanism of neurodegeneration: a proinflammatory cytokine inhibits receptor signaling by a survival peptide. Proc Natl Acad Sci USA 96: 9879-84. (1999).
[124]
Mendham AE, Duffield R, Marino F, Coutts AJ. Small-sided games training reduces CRP, IL-6 and leptin in sedentary, middle-aged men. Eur J Appl Physiol 114: 2289-97. (2014).
[125]
Greiwe JS, Cheng B, Rubin DC, Yarasheski KE, Semenkovich CF. Resistance exercise decreases skeletal muscle tumor necrosis factor alpha in frail elderly humans. FASEB J 15: 475-82. (2001).
[126]
Oztürk C, Ozge A, Yalin OO, Yilmaz IA, Delialioglu N, Yildiz C, et al. The diagnostic role of serum inflammatory and soluble proteins on dementia subtypes: correlation with cognitive and functional decline. Behav Neurol 18: 207-15. (2007).
[127]
Smith LL, Anwar A, Fragen M, Rananto C, Johnson R, Holbert D. Cytokines and cell adhesion molecules associated with high-intensity eccentric exercise. Eur J Appl Physiol 82: 61-7. (2000).
[128]
Balducci S, Zanuso S, Nicolucci A, Fernando F, Cavallo S, Cardelli P, et al. Anti-inflammatory effect of exercise training in subjects with type 2 diabetes and the metabolic syndrome is dependent on exercise modalities and independent of weight loss. Nutr Metab Cardiovasc Dis 20: 608-17. (2010).
[129]
Nieman DC, Davis JM, Henson DA, Walberg-Rankin J, Shute M, Dumke CL, et al. Carbohydrate ingestion influences skeletal muscle cytokine mRNA and plasma cytokine levels after a 3-h run. J Appl Physiol 94: 1917-25. (2003).
[130]
Chan MH, Carey AL, Watt MJ, Febbraio MA. Cytokine gene expression in human skeletal muscle during concentric contraction: evidence that IL-8, like IL-6, is influenced by glycogen availability. Am J Physiol Regul Integr Comp Physiol 287: R322-7. (2004).
[131]
Petersen EW, Carey AL, Sacchetti M, Steinberg GR, Macaulay SL, Febbraio MA, et al. Acute IL-6 treatment increases fatty acid turnover in elderly humans in vivo and in tissue culture in vitro: evidence that IL-6 acts independently of lipolytic hormones. Am J Physiol Endocrinol Metab 288: E155-62. (2005).
[132]
Starkie R, Ostrowski SR, Jauffred S, Febbraio M, Pedersen BK. Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans. FASEB J 17: 884-6. (2003).
[133]
Frydelund-Larsen L, Penkowa M, Akerstrom T, Zankari A, Nielsen S, Pedersen BK. Exercise inducesinterleukin-8 receptor (CXCR2) expression in human skeletal muscle. Exp Physiol 92: 233-40. (2007).
[134]
Craft S. The role of metabolic disorders in Alzheimer disease and vascular dementia: two roads converged. Arch Neurol 66: 300-5. (2009).
[135]
Ostrowski K, Hermann C, Bangash A, Schjerling P, Nielsen JN, Pedersen BK. A trauma-like elevation of plasma cytokines in humans in response to treadmill running. J Physiol 513: 889-94. (1998).
[136]
Riechman SE, Balasekaran G, Roth SM, Ferrell RE. Association of interleukin-15 protein and interleukin-15 receptor genetic variation with resistance exercise training responses. J Appl Physiol 97: 2214-9. (2004).
[137]
Pérez-López A, McKendry J, Martin-Rincon M, Morales-Alamo D, Pérez-Köhler B, Valadés D, et al. Skeletal muscle IL-15/IL-15Rα and myofibrillar protein synthesis after resistance exercise. Scand J Med Sci Sports 28: 116-25. (2018).
[138]
Pérez-López A, Valadés D, Vázquez MC, de Cos Blanco AI, Bujan J, García-Honduvilla N. Serum IL-15 and IL-15Rα levels are decreased in lean and obese physically active humans. Scand J Med Sci Sports 28: 1113-20. (2018).
[139]
Pedersen BK, Bruunsgaard H. Possible beneficial role of exercise in modulating low-grade inflammation in the elderly. Scand J Med Sci Sports 13: 56-62. (2003).
[140]
Arwert LI, Deijen JB, Drent ML. The relation between insulin-like growth factor I levels and cognition in healthy elderly: a meta-analysis. Growth Horm IGF Res 15: 416-22. (2005).
[141]
Burns JM, Cronk BB, Anderson HS, Donnelly JE, Thomas GP, Harsha A, et al. Cardiorespiratory fitness and brain atrophy in early Alzheimer disease. Neurology 71: 210-6. (2008).
[142]
Honea RA, Thomas GP, Harsha A, Anderson HS, Donnelly JE, Brooks WM, et al. Cardiorespiratory fitness and preserved medial temporal lobe volume in Alzheimer disease. Alzheimer Dis Assoc Disord 23: 188-97. (2009).


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 16
ISSUE: 4
Year: 2019
Page: [316 - 332]
Pages: 17
DOI: 10.2174/1567205016666190228125429
Price: $58

Article Metrics

PDF: 35
HTML: 3
EPUB: 1
PRC: 1