Aerobic exercise improves cognition for older adults with glucose intolerance, a risk factor for Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 22, Issue 2, 2010, Pages 569-579

  Baker, Laura D ^a,b   Frank, Laura L ^a,b   Foster Schubert, Karen ^a,c   Green, Pattie S ^a,d   Wilkinson, Charles W ^a,b   McTiernan, Anne ^a,c   Cholerton, Brenna A ^a,b   Plymate, Stephen R ^a,b   Fishel, Mark A ^a,b   Watson, G Stennis ^a,b   Duncan, Glen E ^e   Mehta, Pankaj D ^f   Craft, Suzanne ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

^d VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

Author keywords

Aerobic exercise; Alzheimer's disease; cognition; dementia; diabetes; executive function; glucose intolerance; prediabetes

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; BRAIN DERIVED NEUROTROPHIC FACTOR; GLUCOSE; HYDROCORTISONE; INSULIN; SOMATOMEDIN C;

ADULT; AEROBIC EXERCISE; AGED; ALZHEIMER DISEASE; ARTICLE; BODY FAT DISTRIBUTION; BODY MASS; CLINICAL ARTICLE; COGNITION; CORRELATION ANALYSIS; FEMALE; GLUCOSE CLAMP TECHNIQUE; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; HUMAN; HYDROCORTISONE BLOOD LEVEL; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; MALE; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; MULTIVARIATE ANALYSIS OF COVARIANCE; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PSYCHOLOGIC ASSESSMENT; PSYCHOLOGIC TEST; RANDOMIZED CONTROLLED TRIAL; RISK FACTOR; STRETCHING EXERCISE; TREADMILL EXERCISE; VERBALIZATION; WORD LIST RECALL;

EID: 78650827898     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-100768     Document Type: Article

References (74)

1. Messier C, Tsiakas M, Gagnon M, Desrochers A, Awad N (2003) Effect of age and glucoregulation on cognitive performance. Neurobiol Aging 24, 985-1003.
2. Messier C, Tsiakas M, Gagnon M, Desrochers A (2010) Effect of age and glucoregulation on cognitive performance. J Clin Exp Neuropsychol 5, 1-13.
3. Vanhanen M, Koivisto K, Kuusisto J, Mykkanen L, Helkala E-L, Hanninen T, Riekkinen P, Soininen H, Laakso M (1998) Cognitive function in an elderly population with persistent impaired glucose tolerance. Diabetes Care 21, 398-402.
4. Expert Committee on the Diagnosis and Classification of Diabetes Mellitus (2003) Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care 26(Suppl 1), S5-20.
5. Awad N, Gagnon M, Messier C (2004) The relationship between impaired glucose tolerance, type 2 diabetes, and cognitive function. J Clin Exp Neuropsychol 26, 1044-1080.
6. Baquer NZ, Taha A, Kumar P, McLean P, Cowsik SM, Kale RK, Singh R, Sharma D (2009) A metabolic and functional overview of brain aging linked to neurological disorders. Biogerontology 10, 377-413.
7. Biessels GJ, Deary IJ, Ryan CM (2008) Cognition and diabetes: a lifespan perspective. Lancet Neurol 7, 184-190.
8. Craft S (2005) Insulin resistance syndrome and Alzheimer's disease: age-and obesity-related effects on memory, amyloid, and inflammation. Neurobiol Aging 26 (Suppl 1), 65-69.
9. Cukierman T, Gerstein HC, Williamson JD (2005) Cognitive decline and dementia in diabetes-systematic overview of prospective observational studies. Diabetologia 48, 24602469.
10. Lopez OL, Jagust WJ, DeKosky ST, Becker JT, Fitzpatrick A, Dulberg C, Breitner J, Lyketsos C, Jones B, Kawas C, Carlson M, Kuller LH (2003) Prevalence and classification of mild cognitive impairment in the Cardiovascular Health Study Cognition Study: part Arch Neurol 60, 1385-1389.
11. Luchsinger JA, Reitz C, Patel B, Tang MX, Manly JJ, Mayeux R (2007) Relation of diabetes to mild cognitive impairment. Arch Neurol 64, 570-575.
12. Luchsinger JA (2010) Type 2 diabetes and related conditions in relation to dementia: an opportunity for prevention? J Alzheimers Dis 20, 723-723.
13. Diabetes Prevention Program Research Group (2002) The Diabetes Prevention Program: reduction in the incidence oftype 2 diabetes with lifestyle intervention or metformin. NEJM346, 393-403.
14. Craft S (2007) Insulin resistance and Alzheimer's disease pathogenesis: potential mechanisms and implications for treatment. Curr Alzheimer Res 4, 147-152.
15. Gasparini L, Xu H (2003) Potential roles of insulin and IGF-1 in Alzheimer's disease. Trends Neurosci 26, 404-406.
16. Helzner EP, Luchsinger JA, Scarmeas N, Cosentino S, Brick-man AM, Glymour MM, Stern Y (2009) Contribution of vascular risk factors to the progression in Alzheimer disease. Arch Neurol 66, 343-348.
17. Kuusisto J, Koivisto K, Mykkanen L, Helkala E-L, Vanhanen M, Hanninen T, Kervinen K, Kesaniemi YA, Riekkinen PJ, Laakso M (1997) Association between features of the insulin resistance syndrome and Alzheimer's disease independently of apolipoprotein E4 phenotype: cross sectional population based study. BMJ 315, 1045-1049.
18. Cotman CW, Berchtold NC, Christie LA (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30, 464-472.
19. Kramer AF, Erickson KI, Colcombe SJ (2006) Exercise, cognition, and the aging brain. J Appl Physiol 101, 1237-1242.
20. Colcombe S, Erickson K, Raz N, Webb A, Cohen N, McAuley E, Kramer A (2003) Aerobic fitness reduces brain tissue loss in aging humans. J Gerontol Med Sci 58A, 176-180.
21. Colcombe SJ, Kramer AF, Erickson KI, Scalf P, McAuley E, Cohen NJ, Webb A, Jerome GJ, Marquez DX, Elavsky S (2004) Cardiovascular fitness, cortical plasticity, and aging. Proc Natl Acad Sci USA 101, 3316-3321.
22. Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, Elavsky S, Marquez DX, Hu L, Kramer AF (2006) Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 61, 1166-1170.
23. Daniels K, Toth J, Jacoby L (2006) The aging of executive functions In Lifespan Cognition: Mechanisms of Change, Bi-alystok E, Craik F, eds, Oxford University Press, New York, New York, pp. 96-111.
24. Baker LD, Frank LL, Foster-Schubert K, Green PS, Wilkinson CW, McTiernan A, Plymate SR, Fishel MA, Watson GS, Cholerton BA, Duncan GE, Mehta PD, Craft S (2010) Effects of aerobic exercise on mild cognitive impairment: A controlled trial. Arch Neurol 67, 1-9.
25. Lautenschlager NT, Cox KL, Flicker L, Foster JK, van Bockxmeer FM, Xiao J, Greenop KR, Almeida OP (2008) Effect of physical activity on cognitive function in older adults at risk for Alzheimer disease: a randomized trial. JAMA 300, 1027-1037.
26. Broe GA, Henderson AS, Creasey H, McCusker E, Korten AE, Jorm AF, Longley W, Anthony JC (1990) A case-control study of Alzheimer's disease in Australia. Neurology 40,1698-1707.
27. Laurin D, Verreault R, Lindsay J, MacPherson K, Rockwood K (2001) Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch Neurol 58, 498-504.
28. Li G, Shen YC, Chen CH, Zhau YW, Li SR, Lu M (1989) An epidemiological survey of age-related dementia in an urban area of Beijing. Acta Psychiatr Scand 79, 557-563.
29. Pate R, Blair S, Durstine J, Eddy D, Hanson P, Painter P, Smith L, Wolfe L (1991), ed. Pate R (Lea and Febiger, Philadelphia, PA).
30. Hagberg J (1994) Exercise assessment of arthritic and elderly individuals. Baillieres Clin Rheumatol 8, 29-52.
31. DeFronzo RA, Tobin JD, Andres R (1979) Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol 237, E214-223.
32. Shibuya-Tayoshi S, Sumitani S, Kikuchi K, Tanaka T, Tayoshi S, Ueno S, Ohmori T (2007) Activation ofthe prefrontal cortex during the Trail-Making Test detected with multichannel near-infrared spectroscopy. Psychiatry Clin Neurosci 61, 616-621.
33. Kramer AF, Hahn S, McAuley E, Cohen NJ, Banich MT, Harrison C, Chason J, Boileau RA, Bardell L, Colcombe A, Vakil E (2001) Exercise, Aging and Cognition: Healthy Body, Healthy Mind? In Human Factors Interventions for the Health Care of Older Adults, Fisk AD, Rogers W, eds, Erlbaum, Hillsdale, N.J.
34. Rogers R, Sahakian B, Hodges J, Polkey C, Kennard C, Robbins T (1998). Dissociating executive mechanisms of task control following frontal lobe damage and Parkinson's disease. Brain 121, 815-842.
35. Golden CJ (1978) Stroop Color and Word Test, Stoelting, Chicago.
36. Spieler DH, Balota DA, Faust ME (1996) Stroop performance in healthy younger and older adults and in individuals with dementia of the Alzheimer's type. J Exp Psychol Hum Percept Perform 22, 461-479.
37. Daigneault S, BraunCM (1993) Working memory and the self-ordered pointing task: Further evidence of early prefrontal decline in normal aging. J Clin ExpNeuropsychol 16, 881-895.
38. Petrides M, Milner B (1982) Deficits on subject-ordered tasks after frontal-and temporal-lobe lesions in man. Neuropsy-chologia 20, 249-262.
39. Lonie JA, Herrmann LL, Tierney KM, Donaghey C, O'Carroll R, Lee A, Ebmeier KP (2009) Lexical and semantic fluency discrepancy scores in aMCI and early Alzheimer's disease. J Neuropsychol 3, 79-92.
40. Nutter-Upham KE, Saykin AJ, Rabin LA, Roth RM, Wishart HA, Pare N, Flashman LA (2008) Verbal fluency performance in amnestic MCI and older adults with cognitive complaints. Arch Clin Neuropsychol 23, 229-241.
41. Chodosh J, Reuben D, Albert M, Seeman T (2002) Predicting cognitive impairment in high-functioning community-dwelling older persons: MacArthur Studies of Successful Aging. JAm Geriatr Soc 50, 1051-1060.
42. Craft S, Asthana S, Cook DG, Baker LD, Cherrier M, Purganan K, Wait C, Petrova A, Latendresse S, Watson GS, Newcomer JW, Schellenberg GD, Krohn AJ (2003) Insulin dose-response effects on memory and plasma amyloid precursor protein in Alzheimer's disease: interactions with apolipoprotein E genotype. Psychoneuroendocrinology 28, 809-822.
43. Blacker D, Lee H, Muzikansky A, Martin EC, Tanzi R, McArdle JJ, Moss M, Albert M (2007) Neuropsychological measures in normal individuals that predict subsequent cognitive decline. ArchNeurol 64, 862-871.
44. Fujimura H, Altar CA, Chen R, Nakamura T, Nakahashi T, Kambayashi J, Sun B, Tandon NN (2002) Brain-derived neu-rotrophic factor is stored in human platelets and released by agonist stimulation. Thromb Haemost 87, 728-734.
45. Mehta PD, Pirttila T, Mehta SP, Sersen EA, Aisen PS, Wisniewski HM (2000) Plasma and cerebrospinal fluid levels of amyloid beta proteins 1-40 and 1-42 in Alzheimer disease. ArchNeurol 57, 100-105.
46. StataCorp (2007) (StataCorp, College Station, TX).
47. Colcombe S, Kramer A (2003) Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol Sci 14, 125-130.
48. Manschot SM, Brands AM, van der Grond J, Kessels RP, Algra A, Kappelle LJ, Biessels GJ (2006) Brain magnetic resonance imaging correlates of impaired cognition in patients with type 2 diabetes. Diabetes 55, 1106-1113.
49. Manschot SM, Biessels GJ, de Valk H, Algra A, Rutten GE, van der Grond J, Kappelle LJ (2007) Metabolic and vascular determinants of impaired cognitive performance and abnormalities on brain magnetic resonance imaging in patients with type 2 diabetes. Diabetologia 50, 2388-2397.
50. Thabit H, Kennelly SM, Bhagarva A, Ogunlewe M, McCormack PM, McDermott JH, Sreenan S (2009) Utilization of Frontal Assessment Battery and Executive Interview 25 in assessing for dysexecutive syndrome and its association with diabetes self-care in elderly patients with type 2 diabetes mel-litus. Diabetes Res Clin Pract 86, 208-212.
51. Chang YL, Jacobson MW, Fennema-Notestine C, Hagler DJ, Jr., Jennings RG, Dale AM, McEvoy LK (2009) Level of executive function influences verbal memory in amnestic mild cognitive impairment and predicts prefrontal and posterior cingulate thickness. Cereb Cortex. 20, 1305-1313.
52. Chen TF, Chen YF, Cheng TW, Hua MS, Liu HM, Chiu MJ (2009) Executive dysfunction and periventricular diffusion tensor changes in amnesic mild cognitive impairment and early Alzheimer's disease. Hum Brain Mapp 30, 3826-3836.
53. Messier C, Gagnon M (2009) Cognitive decline associated with dementia and type 2 diabetes: the interplay of risk factors. Diabetologia 52, 2471-2474.
54. Ott A, Stolk RP, van Harskamp F, Pols HA, Hofman A, Breteler MM (1999) Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology 53, 1937-1942.
55. Yaffe K, Blackwell T, Kanaya AM, Davidowitz N, Barrett-Connor E, Krueger K (2004) Diabetes, impaired fasting glucose, and development ofcognitive impairment in older women. Neurology 63, 658-663.
56. Luchsinger JA, Tang MX, Shea S, Mayeux R (2004) Hyperin-sulinemia and risk of Alzheimer disease. Neurology 63, 11871192.
57. Peila R, Rodriguez BL, White LR, Launer LJ (2004) Fasting insulin and incident dementia in an elderly population of Japanese-American men. Neurology 63, 228-233.
58. Gomez-Pinilla F, Vaynman S, Ying Z (2008) Brain-derived neurotrophic factor functions as a metabotrophin to mediate the effects of exercise on cognition. Eur J Neurosci 28, 2278-2287.
59. Bruehl H, Wolf OT, Sweat V, Tirsi A, Richardson S, Convit A (2009) Modifiers of cognitive function and brain structure in middle-aged and elderly individuals with type 2 diabetes mellitus. Brain Res 1280, 186-194.
60. Ryan CM, Freed MI, Rood JA, Cobitz AR, Waterhouse BR, Strachan MW (2006) Improving metabolic control leads to better working memory in adults with type 2 diabetes. Diabetes Care 29, 345-351.
61. Messier C, Teutenberg K (2005) The role of insulin, insulin growth factor, and insulin-degrading enzyme in brain aging and Alzheimer's disease. Neural Plast 12, 311-328.
62. Abbatecola AM, Paolisso G, Lamponi M, Bandinelli S, Lau-retani F, Launer L, Ferrucci L (2004) Insulin resistance and executive dysfunction in older persons. J Am Geriatr Soc 52, 1713-1718.
63. Kaplan RJ, Greenwood CE, Winocur G, Wolever TM (2000) Cognitive performance is associated with glucose regulation in healthy elderly persons and can be enhanced with glucose and dietary carbohydrates. AmJ Clin Nutr 72, 825-836.
64. Vanhanen M, Koivisto K, Karjalainen L, Helkala EL, Laakso M, Soininen H, Riekkinen P, Sr. (1997) Risk for non-insulin-dependent diabetes in the normoglycaemic elderly is associated with impaired cognitive function. Neuroreport 8, 15271530.
65. Campbell JJ, 3rd, Coffey CE (2001) Neuropsychiatric significance of subcortical hyperintensity. J Neuropsychiatry Clin Neurosci 13, 261-288.
66. Jellinger KA (2002) Alzheimer disease and cerebrovascular pathology: an update. J Neural Transm 109, 813-836.
67. Stopa EG, Butala P, Salloway S, Johanson CE, Gonzalez L, Tavares R, Hovanesian V, Hulette CM, Vitek MP, Cohen RA (2008) Cerebral cortical arteriolar angiopathy, vascular beta-amyloid, smooth muscle actin, Braak stage, and APOE genotype. Stroke 39, 814-821.
68. van Praag H, Shubert T, Zhao C, Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25, 8680-8685.
69. Mayeux R, Tang MX, Jacobs DM, Manly J, Bell K, Merchant C, Small SA, Stern Y, Wisniewski HM, Mehta PD (1999) Plasma amyloid beta-peptide 1-42 and incipient Alzheimer's disease. Ann Neurol 46, 412-416.
70. Cao D, Lu H, Lewis TL, Li L (2007) Intake of sucrose-sweetened water induces insulin resistance and exacerbates memory deficits and amyloidosis in a transgenic mouse model of Alzheimer disease. JBiol Chem 282, 36275-36282.
71. Takeda S, Sato N, Uchio-Yamada K, Sawada K, Kunieda T, Takeuchi D, Kurinami H, Shinohara M, Rakugi H, Morishita R (2009) Elevation of plasma beta-amyloid level by glucose loading in Alzheimer mouse models. Biochem Biophys Res Commun 385, 193-197.
72. Adlard PA, Perreau VM, Pop V, Cotman CW (2005) Voluntary exercise decreases amyloid load in a transgenic model of Alzheimer's disease. J Neurosci 25, 4217-4221.
73. Nichol KE, Poon WW, Parachikova AI, Cribbs DH, Glabe CG, Cotman CW (2008). Exercise alters the immune profile in Tg2576 Alzheimer mice toward a response coincident with improved cognitive performance and decreased amyloid. J Neuroinflammation 5, 13.
74. Um HS, Kang EB, Leem YH, Cho IH, Yang CH, Chae KR, Hwang DY, Cho JY (2008) Exercise training acts as a therapeutic strategy for reduction ofthe pathogenic phenotypes for Alzheimer's disease in an NSE/APPsw-transgenic model. Int J Mol Med 22, 529-539.