Resistance training does not have an effect on cognition or related serum biomarkers in nonagenarians: A randomized controlled trial

International Journal of Sports Medicine

Volumn 36, Issue 1, 2015, Pages 54-60

  Ruiz, Jonatan R ^a   Gil Bea, F ^b   Bustamante Ara, N ^c   Rodriguez Romo G ^d   Fiuza Luces, C ^c   Serra Rexach, J A ^e   Cedazo Minguez, A ^f   Lucia, A ^c  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

^c UNIVERSIDAD EUROPEA DE MADRID   (Spain)

^d UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

^e HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^f KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Cognitive decline; Cognitive function; Elderly; Mini mental state examination; Physical activity

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BIOLOGICAL MARKER; BRAIN DERIVED NEUROTROPHIC FACTOR; DIPEPTIDYL CARBOXYPEPTIDASE; EPIDERMAL GROWTH FACTOR; PLASMA PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

AGING; BLOOD; COGNITION; CONTROLLED STUDY; FEMALE; HUMAN; MALE; METABOLISM; MUSCLE STRENGTH; PHYSIOLOGY; PSYCHOLOGY; RANDOMIZED CONTROLLED TRIAL; RESISTANCE TRAINING; VERY ELDERLY;

AGED, 80 AND OVER; AGING; AMYLOID BETA-PROTEIN PRECURSOR; BIOLOGICAL MARKERS; BLOOD PROTEINS; BRAIN-DERIVED NEUROTROPHIC FACTOR; COGNITION; EPIDERMAL GROWTH FACTOR; FEMALE; HUMANS; MALE; MUSCLE STRENGTH; PEPTIDYL-DIPEPTIDASE A; RESISTANCE TRAINING; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84920087415     PISSN: 01724622     EISSN: 14393964     Source Type: Journal    
DOI: 10.1055/s-0034-1375693     Document Type: Article

References (63)

1. ACSM. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc 2009; 41: 687-708
2. Adams V, Linke A, Breuckmann F, Leineweber K, Erbs S, Krankel N, Brocker-Preuss M, Woitek F, Erbel R, Heusch G, Hambrecht R, Schuler G, Mohlenkamp S. Circulating progenitor cells decrease immediately after marathon race in advanced-age marathon runners. Eur J Cardiovasc Prev Rehabil 2008; 15: 602-607
3. Akinyemi R O, Mukaetova-Ladinska E B, Attems J, Ihara M, Kalaria R N. Vascular risk factors and neurodegeneration in ageing related dementias: Alzheimer's disease and vascular dementia. Curr Alzheimer Res 2013; 10: 642-653
4. Angevaren M, Aufdemkampe G, Verhaar H J, Aleman A, Vanhees L. Physical activity and enhanced fitness to improve cognitive function in older people without known cognitive impairment. Cochrane Database Syst Rev 2008, 10.1002/14651858.CD005381.pub3: CD005381
5. Bjorkqvist M, Ohlsson M, Minthon L, Hansson O. Evaluation of a previously suggested plasma biomarker panel to identify Alzheimer's disease. PLoS One 2012; 7: e29868
6. Cassilhas R C, Viana V A, Grassmann V, Santos R T, Santos R F, Tufik S, Mello M T. The impact of resistance exercise on the cognitive function of the elderly. Med Sci Sports Exerc 2007; 39: 1401-1407
7. Castellano V, White L J. Serum brain-derived neurotrophic factor response to aerobic exercise in multiple sclerosis. J Neurol Sci 2008; 269: 85-91
8. Cedazo-Minguez A, Winblad B. Biomarkers for Alzheimer's disease and other forms of dementia: clinical needs, limitations and future aspects. Exp Gerontol 2010; 45: 5-14
9. Chasseigneaux S, Allinquant B. Functions of Abeta, sAPPalpha and sAPPbeta: similarities and differences. J Neurochem 2012; 120 (Suppl 1): 99-108
10. Chen-Plotkin A S, Hu W T, Siderowf A, Weintraub D, Goldmann Gross R, Hurtig H I, Xie S X, Arnold S E, Grossman M, Clark C M, Shaw L M, McCluskey L, Elman L, Van Deerlin V M, Lee V M, Soares H, Trojanowski J Q. Plasma epidermal growth factor levels predict cognitive decline in Parkinson disease. Ann Neurol 2011; 69: 655-663
11. Coelho F G, Gobbi S, Andreatto C A, Corazza D I, Pedroso R V, Santos-Galduroz R F. Physical exercise modulates peripheral levels of brain-derived neurotrophic factor (BDNF): a systematic review of experimental studies in the elderly. Arch Gerontol Geriatr 2013; 56: 10-15
12. Coelho F M, Pereira D S, Lustosa L P, Silva J P, Dias J M, Dias R C, Queiroz B Z, Teixeira A L, Teixeira M M, Pereira L S. Physical therapy intervention (PTI) increases plasma brain-derived neurotrophic factor (BDNF) levels in non-frail and pre-frail elderly women. Arch Gerontol Geriatr 2012; 54: 415-420
13. Colcombe S, Kramer A F. Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci 2003; 14: 125-130
14. Correia P R, Pansani A, Machado F, Andrade M, Silva A C, Scorza F A, Cavalheiro E A, Arida R M. Acute strength exercise and the involvement of small or large muscle mass on plasma brain-derived neurotrophic factor levels. Clinics (Sao Paulo) 2010; 65: 1123-1126
15. Cotman C W, Berchtold N C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 2002; 25: 295-301
16. de Salles B F, Simao R, Fleck S J, Dias I, Kraemer-Aguiar L G, Bouskela E. Effects of resistance training on cytokines. Int J Sports Med 2010; 31: 441-450
17. Denkinger M D, Nikolaus T, Denkinger C, Lukas A. Physical activity for the prevention of cognitive decline: current evidence from observational and controlled studies. Z Gerontol Geriatr 2012; 45: 11-16
18. Direk N, Koudstaal P J, Hofman A, Ikram M A, Hoogendijk W J, Tiemeier H. Cerebral hemodynamics and incident depression: the Rotterdam Study. Biol Psychiatry 2012; 72: 318-323
19. Direk N, Schrijvers E M, de Bruijn R F, Mirza S, Hofman A, Ikram M A, Tiemeier H. Plasma amyloid beta, depression, and dementia in com-munity- dwelling elderly. J Psychiatr Res 2013; 47: 479-485
20. Etnier J L, Nowell P M, Landers D M, Sibley B A. A meta-regression to examine the relationship between aerobic fitness and cognitive performance. Brain Res Rev 2006; 52: 119-130
21. Fatouros I, Chatzinikolaou A, Paltoglou G, Petridou A, Avloniti A, Jamurtas A, Goussetis E, Mitrakou A, Mougios V, Lazaropoulou C, Margeli A, Papassotiriou I, Mastorakos G. Acute resistance exercise results in catecholaminergic rather than hypothalamic-pituitary-adrenal axis stimulation during exercise in young men. Stress 2010; 13: 461-468
22. Foster P P, Rosenblatt K P, Kuljis R O. Exercise-induced cognitive plasticity, implications for mild cognitive impairment and Alzheimer's disease. Front Neurol 2011; 2: 28
23. Goekint M, De Pauw K, Roelands B, Njemini R, Bautmans I, Mets T, Meeusen R. Strength training does not influence serum brain-derived neurotrophic factor. Eur J Appl Physiol 2010; 110: 285-293
24. Gomez-Pinilla F, Ying Z, Roy R R, Molteni R, Edgerton V R. Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol 2002; 88: 2187-2195
25. Gonzalo-Ruiz A, Gonzalez I, Sanz-Anquela J M. Effects of beta-amyloid protein on serotoninergic, noradrenergic, and cholinergic markers in neurons of the pontomesencephalic tegmentum in the rat. J Chem Neuroanat 2003; 26: 153-169
26. Hamer M, Chida Y. Physical activity and risk of neurodegenerative disease: a systematic review of prospective evidence. Psychol Med 2009; 39: 3-11
27. Harriss D J, Atkinson G. Ethical standards in sport and exercise science research: 2014 update. Int J Sports Med 2013; 34: 1025-1028
28. Heyn P C, Johnson K E, Kramer A F. Endurance and strength training outcomes on cognitively impaired and cognitively intact older adults: a meta-analysis. J Nutr Health Aging 2008; 12: 401-409
29. Higashi Y, Yoshizumi M. Exercise and endothelial function: role of endothelium-derived nitric oxide and oxidative stress in healthy subjects and hypertensive patients. Pharmacol Ther 2004; 102: 87-96
30. 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 2013, doi: 10.1111/sms.12069
31. Kimura K, Obuchi S, Arai T, Nagasawa H, Shiba Y, Watanabe S, Kojima M. The influence of short-term strength training on health-related quality of life and executive cognitive function. J Physiol Anthropol 2010; 29: 95-101
32. Kitazume S, Yoshihisa A, Yamaki T, Oikawa M, Tachida Y, Ogawa K, Imamaki R, Hagiwara Y, Kinoshita N, Takeishi Y, Furukawa K, Tomita N, Arai H, Iwata N, Saido T, Yamamoto N, Taniguchi N. Soluble amyloid precursor protein 770 is released from inflamed endothelial cells and activated platelets: a novel biomarker for acute coronary syndrome. J Biol Chem 2012; 287: 40817-40825
33. Kramer A F, Hahn S, Cohen N J, Banich M T, McAuley E, Harrison C R, Chason J, Vakil E, Bardell L, Boileau R A, Colcombe A. Ageing, fitness and neurocognitive function. Nature 1999; 400: 418-419
34. Lachman M E, Neupert S D, Bertrand R, Jette A M. The effects of strength training on memory in older adults. J Aging Phys Act 2006; 14: 59-73
35. Lautenschlager N T, Cox K L, Flicker L, Foster J K, van Bockxmeer F M, Xiao J, Greenop K R, Almeida O P. Effect of physical activity on cognitive function in older adults at risk for Alzheimer disease: a randomized trial. JAMA 2008; 300: 1027-1037
36. Levinger I, Goodman C, Matthews V, Hare D L, Jerums G, Garnham A, Selig S. BDNF, metabolic risk factors, and resistance training in middleaged individuals. Med Sci Sports Exerc 2008; 40: 535-541
37. Li N C, Lee A, Whitmer R A, Kivipelto M, Lawler E, Kazis L E, Wolozin B. Use of angiotensin receptor blockers and risk of dementia in a predominantly male population: prospective cohort analysis. BMJ 2010; 340: b5465
38. Liu-Ambrose T, Nagamatsu L S, Graf P, Beattie B L, Ashe M C, Handy T C. Resistance training and executive functions: a 12-month randomized controlled trial. Arch Intern Med 2010; 170: 170-178
39. Loffler J, Huber G. Beta-amyloid precursor protein isoforms in various rat brain regions and during brain development. J Neurochem 1992; 59: 1316-1324
40. Lucia A, Ruiz J R. Exercise is beneficial for patients with Alzheimer's disease: a call for action. Br J Sports Med 2011; 45: 468-469
41. Macaluso F, Myburgh K H. Current evidence that exercise can increase the number of adult stem cells. J Muscle Res Cell Motil 2012; 33: 187-198
42. Paganelli R, Di Iorio A, Patricelli L, Ripani F, Sparvieri E, Faricelli R, Iarlori C, Porreca E, Di Gioacchino M, Abate G. Proinflammatory cytokines in sera of elderly patients with dementia: levels in vascular injury are higher than those of mild-moderate Alzheimer's disease patients. Exp Gerontol 2002; 37: 257-263
43. Park K M, Bowers W J. Tumor necrosis factor-alpha mediated signaling in neuronal homeostasis and dysfunction. Cell Signal 2010; 22: 977-983
44. Pedersen B K, Febbraio M A. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 2008; 88: 1379-1406
45. Perrig-Chiello P, Perrig W J, Ehrsam R, Staehelin H B, Krings F. The effects of resistance training on well-being and memory in elderly volunteers. Age Ageing 1998; 27: 469-475
46. Rasmussen P, Brassard P, Adser H, Pedersen M V, Leick L, Hart E, Secher N H, Pedersen B K, Pilegaard H. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp Physiol 2009; 94: 1062-1069
47. Ray S, Britschgi M, Herbert C, Takeda-Uchimura Y, Boxer A, Blennow K, Friedman L F, Galasko D R, Jutel M, Karydas A, Kaye J A, Leszek J, Miller B L, Minthon L, Quinn J F, Rabinovici G D, Robinson W H, Sabbagh M N, So Y T, Sparks D L, Tabaton M, Tinklenberg J, Yesavage J A, Tibshirani R, Wyss-Coray T. Classification and prediction of clinical Alzheimer's diagnosis based on plasma signaling proteins. Nat Med 2007; 13: 1359-1362
48. Roy S, Rauk A. Alzheimer's disease and the 'ABSENT' hypothesis: mechanism for amyloid beta endothelial and neuronal toxicity. Med Hypotheses 2005; 65: 123-137
49. Rubio-Perez J M, Morillas-Ruiz JM. A review: inflammatory process in Alzheimer's disease, role of cytokines. Scient World J 2012; 2012: 756357.
50. 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 2009; 41: 250-254
51. Schulz K H, Gold S M, Witte J, Bartsch K, Lang U E, Hellweg R, Reer R, Braumann K M, Heesen C. Impact of aerobic training on immune-endocrine parameters, neurotrophic factors, quality of life and coordinative function in multiple sclerosis. J Neurol Sci 2004; 225: 11-18
52. Seifert T, Brassard P, Wissenberg M, Rasmussen P, Nordby P, Stallknecht B, Adser H, Jakobsen A H, Pilegaard H, Nielsen H B, Secher NH.. Endurance training enhances BDNF release from the human brain. Am J Physiol 2010; 298: R372-R377
53. Selkoe D J, Podlisny M B, Joachim C L, Vickers E A, Lee G, Fritz L C, Oltersdorf T. Beta-amyloid precursor protein of Alzheimer disease occurs as 110-to 135-kilodalton membrane-associated proteins in neural and nonneural tissues. Proc Natl Acad Sci USA 1988; 85: 7341-7345
54. Serra-Rexach J A, Ruiz J R, Bustamante-Ara N, Villaran M H, Gil P G, Sanz Ibanez M J, Sanz N B, Santamaria V O, Sanz N G, Prada A B, Gallardo C, Romo G R, Lucia A. Health enhancing strength training in nonagenarians (STRONG): rationale, design and methods. BMC Public Health 2009; 9: 152
55. Singh M, Meyer E M, Simpkins J W. The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats. Endocrinology 1995; 136: 2320-2324
56. Smith P J, Blumenthal J A, Hoffman B M, Cooper H, Strauman T A, Welsh-Bohmer K, Browndyke J N, Sherwood A. Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosom Med 2010; 72: 239-252
57. Suijo K, Inoue S, Ohya Y, Odagiri Y, Takamiya T, Ishibashi H, Itoh M, Fujieda Y, Shimomitsu T. Resistance exercise enhances cognitive function in mouse. Int J Sports Med 2013; 34: 368-375
58. Tsutsumi T, Don B M, Zaichkowsky L D, Delizonna L L. Physical fitness and psychological benefits of strength training in community dwelling older adults. Appl Human Sci 1997; 16: 257-266
59. van Uffelen J G, Chinapaw M J, van Mechelen W, Hopman-Rock M. Walking or vitamin B for cognition in older adults with mild cognitive impairment? A randomised controlled trial. Br J Sports Med 2008; 42: 344-351
60. Yang Y H, Liu C K. Angiotensin-converting enzyme gene in Alzheimer's disease. Tohoku J Exp Med 2008; 215: 295-298
61. Yarrow J F, White L J, McCoy S C, Borst S E. Training augments resistance exercise induced elevation of circulating brain derived neurotrophic factor (BDNF). Neurosci Lett 2010; 479: 161-165
62. Zoladz J A, Pilc A. The effect of physical activity on the brain derived neurotrophic factor: from animal to human studies. J Physiol Pharmacol 2010; 61: 533-541
63. Zoladz J A, 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 2008; 59 (Suppl 7 ): 119-132