Diabetes is associated with cerebrovascular but not Alzheimer's disease neuropathology

Alzheimer's and Dementia

Volumn 12, Issue 8, 2016, Pages 882-889

  Abner, Erin L ^a,b   Nelson, Peter T ^a   Kryscio, Richard J ^a,b   Schmitt, Frederick A ^a   Fardo, David W ^a,b   Woltjer, Randall L ^c,d   Cairns, Nigel J ^e,f   Yu, Lei ^g,h   Dodge, Hiroko H ^c,d   Xiong, Chengjie ^e,f   Masaki, Kamal ⁱ   Tyas, Suzanne L ^j   Bennett, David A ^g,h   Schneider, Julie A ^g,h   Arvanitakis, Zoe ^g,h  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY COLLEGE OF PUBLIC HEALTH   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f WASHINGTON UNIVERSITY   (United States)

^g RUSH UNIVERSITY MEDICAL CENTER   (United States)

^h RUSH UNIVERSITY MEDICAL CENTER   (United States)

ⁱ UNIVERSITY OF HAWAII   (United States)

^j UNIVERSITY OF WATERLOO   (Canada)

more..

Author keywords

Alzheimer; Autopsy; Cerebrovascular; Cognition; Diabetes; Infarcts; Neuropathology

Indexed keywords

ANTIDIABETIC AGENT;

AGED; ALZHEIMER DISEASE; ARTICLE; AUTOPSY; BRAIN INFARCTION; CEREBROVASCULAR DISEASE; CLINICAL EVALUATION; COGNITION; COGNITION ASSESSMENT; CONTROLLED STUDY; DEATH; DIABETES MELLITUS; DISEASE ASSOCIATION; FEMALE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MINI MENTAL STATE EXAMINATION; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; PRIORITY JOURNAL; SENILE PLAQUE; VERY ELDERLY; ANIMAL; BRAIN; COGNITION DISORDERS; COHORT ANALYSIS; DIABETIC COMPLICATION; MENTAL HEALTH; NEUROPSYCHOLOGICAL TEST; PATHOLOGY; PATHOPHYSIOLOGY; STATISTICAL MODEL;

AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; AUTOPSY; BRAIN; BRAIN INFARCTION; COGNITION DISORDERS; COHORT STUDIES; DIABETES COMPLICATIONS; DIABETES MELLITUS; FEMALE; HUMANS; LOGISTIC MODELS; MALE; MENTAL STATUS SCHEDULE; NEUROFIBRILLARY TANGLES; NEUROPSYCHOLOGICAL TESTS;

EID: 84977616475     PISSN: 15525260     EISSN: 15525279     Source Type: Journal    
DOI: 10.1016/j.jalz.2015.12.006     Document Type: Article

References (48)

1. [1] Matsuzaki, T., Sasaki, K., Tanizaki, Y., Hata, J., Fujimi, K., Matsui, Y., et al. Insulin resistance is associated with the pathology of Alzheimer disease: The Hisayama study. Neurology 75 (2010), 764–770.
2. [2] Cholerton, B., Baker, L.D., Craft, S., Insulin, cognition, and dementia. Eur J Pharmacol 719 (2013), 170–179.
3. [3] Bonfim, T.R., Forny-Germano, L., Sathler, L.B., Brito-Moreira, J., Houzel, J.C., Decker, H., et al. An anti-diabetes agent protects the mouse brain from defective insulin signaling caused by Alzheimer's disease-associated Aβ oligomers. J Clin Invest 122 (2012), 1339–1353.
4. [4] Crane, P.K., Walker, R., Hubbard, R.A., Li, G., Nathan, D.M., Zheng, H., et al. Glucose levels and risk of dementia. N Engl J Med 369 (2013), 540–548.
5. [5] de la Monte, S.M., Wands, J.R., Alzheimer's disease is Type 3 diabetes—Evidence reviewed. J Diabetes Sci Technol 3 (2008), 1101–1113.
6. [6] Luchsinger, J.A., Tang, M.X., Stern, Y., Shea, S., Mayeux, R., Diabetes mellitus and risk of Alzheimer's disease and dementia with stroke in a multiethnic cohort. Am J Epidemiol 154 (2001), 635–641.
7. [7] Peila, R., Rodriguez, B.L., Launer, L.J., Type 2 diabetes, APOE gene, and the risk for dementia and related pathologies. The Honolulu-Asia Aging Study. Diabetes 51 (2002), 1256–1262.
8. [8] Irie, F., Fitzpatrick, A.L., Lopez, O.L., Kuller, L.H., Peila, R., Newman, A.B., et al. Enhanced risk for Alzheimer disease in persons with type 2 diabetes and APOE epsilon4: The Cardiovascular Health Study Cognition Study. Arch Neurol 65 (2008), 89–93.
9. [9] Ahtiluoto, S., Polvikoski, T., Peltonen, M., Solomon, A., Tuomilehto, J., Winblad, B., et al. Diabetes, Alzheimer disease, and vascular dementia. A population-based neuropathologic study. Neurology 75 (2010), 1195–1202.
10. [10] Reiman, E.M., Chen, K., Alexander, G.E., Caselli, R.J., Bandy, D., Osborne, D., et al. Functional brain abnormalities in young adults at genetic risk for late-onset Alzheimer's dementia. Proc Natl Acad Sci U S A 101 (2004), 284–289.
11. [11] Willette, A.A., Johnson, S.C., Birdsill, A.C., Sager, M.A., Christian, B., Baker, L.D., et al. Insulin resistance predicts brain amyloid deposition in middle-aged adults. Alzheimers Dement 11 (2015), 504–510.
12. [12] Thambisetty, M., Metter, E.J., Yang, A., Dolan, H., Marano, C., Zonderman, A.B., et al. Glucose intolerance, insulin resistance and Alzheimer's disease pathology in the Baltimore Longitudinal Study of Aging. JAMA Neurol 70 (2013), 1167–1172.
13. [13] Starks, E.J., O'Grady, J.P., Hoscheidt, S.M., Racine, A.M., Carlsson, C.M., Zetterberg, H., et al. Insulin resistance is associated with higher cerebrospinal fluid tau levels in asymptomatic APOE ε4 carriers. J Alzheimers Dis 46 (2015), 525–533.
14. [14] Talbot, K., Wang, H., Kazi, H., Han, L., Bakshi, K.P., Stucky, A., et al. Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Invest 122 (2012), 1316–1338.
15. [15] Heitner, J., Dickson, D., Diabetics do not have increased Alzheimer-type pathology compared with age-matched control subjects. A retrospective postmortmem immunocytochemical and histofluorescent study. Neurology 49 (1997), 1306–1311.
16. [16] Beeri, M.S., Silverman, J.M., Davis, K.L., Marin, D., Grossman, H.Z., Schmeidler, J., et al. Type 2 diabetes is negatively associated with Alzheimer's disease neuropathology. J Gerontol A Biol Sci Med Sci 60 (2005), 471–475.
17. [17] Sonnen, J.A., Larson, E.B., Brickell, K., Crane, P.K., Woltjer, R., Montine, T.J., et al. Different patterns of cerebral injury in dementia with or without diabetes. Arch Neurol 66 (2009), 315–322.
18. [18] Janson, J., Laedtke, T., Parisi, J.E., O'Brien, P., Petersen, R.C., Butler, P.C., Increased risk of type 2 diabetes in Alzheimer's disease. Diabetes 53 (2004), 474–481.
19. [19] Wolf, P.A., D'Agostino, R.B., Belanger, A.J., Kannel, W.B., Probability of stroke: A risk profile from the Framingham Study. Stroke 22 (1991), 312–318.
20. [20] Rastas, S., Pirttila, T., Mattila, K., Verkkoniemi, A., Juva, K., Niinisto, L., et al. Vascular risk factors and dementia in the general population aged <85 years. Prospective population-based study. Neurobiol Aging 31 (2010), 1–7.
21. [21] Brundel, M., Reijmer, Y.D., van Veluw, S.J., Kujif, H.J., Luijten, P.R., Kappelle, L.J., et al. Cerebral microvascular lesions on high-resolution 7-Tesla MRI in patients with type 2 diabetes. Diabetes 63 (2014), 3523–3529.
22. [22] Abner, E.L., Schmitt, F.A., Nelson, P.T., Lou, W., Wan, L., Gauriglia, R., et al. The Statistical Modeling of Aging and Risk of Transition Project: Data collection and harmonization across 11 longitudinal cohort studies of aging, cognition, and dementia. Obs Stud 1 (2015), 56–73.
23. [23] Braak, H., Braak, E., Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82 (1991), 239–259.
24. [24] Mirra, S.S., Heyman, A., McKeel, D., Sumi, S.M., Crain, B.J., Brownlee, L.M., et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41 (1991), 479–486.
25. [25] Gelber, R.P., Launer, L.J., White, L.R., The Honolulu-Asia Aging Study: Epidemiologic and neuropathologic research on cognitive impairment. Curr Alzheimer Res 9 (2012), 664–672.
26. [26] Green, M.S., Kaye, J.A., Ball, M.J., The Oregon Brain Aging Study: Neuropathology accompanying healthy aging in the oldest old. Neurology, 54, 2000, 105.
27. [27] Kaye, J., Michael, Y., Calvert, J., Leahy, M., Crawford, D., Kramer, P., Exceptional brain aging in a rural population-based cohort. J Rural Health 25 (2009), 320–325.
28. [28] Bennett, D.A., Schneider, J.A., Buchman, A.S., Mendes de Leon, C., Bienias, J.L., Wilson, R.S., The Rush Memory and Aging Project: Study design and baseline characteristics of the study cohort. Neuroepidemiology 25 (2005), 163–175.
29. [29] Bennett, D.A., Schneider, J.A., Buchman, A.S., Barnes, L.L., Boyle, P.A., Wilson, R.S., Overview and findings from the Rush Memory and Aging Project. Curr Alzheimer Res 9 (2012), 648–665.
30. [30] Berg, L., McKeel, D.W., Miller, J.P., Storandt, M., Rubin, E.H., Morris, J.C., et al. Clinicopathologic studies in cognitively healthy aging and Alzheimer's disease. Relation of histologic markers to dementia severity, age, sex, and apolipoprotein E genotype. Arch Neurol 55 (1998), 326–335.
31. [31] Schmitt, F.A., Nelson, P.T., Abner, E., Scheff, S., Jicha, G.A., Smith, C., et al. University of Kentucky Sanders-Brown Health Brain Aging volunteers: Donor characteristics, procedures, and neuropathology. Curr Alzheimer Res 9 (2012), 724–733.
32. [32] Arvanitakis, Z., Schneider, J.A., Wilson, R.S., Li, Y., Arnold, S.E., Wang, Z., et al. Diabetes is related to cerebral infarction but to AD pathology in older persons. Neurology 67 (2006), 1960–1965.
33. [33] Arvanitakis, Z., Bennett, D.A., Wilson, R.S., Barnes, L.L., Diabetes and cognitive systems in older black and white persons. Alzheimer Dis Assoc Disord 24 (2010), 37–42.
34. [34] Nelson, P.T., Smith, C.D., Abner, E.L., Schmitt, F.A., Scheff, S.W., Davis, G.J., et al. Human cerebral neuropathology of type 2 diabetes mellitus. Biochim Biophys Acta 1792 (2009), 454–469.
35. [35] Schütt, M., Fach, E., Seufert, J., Kerner, W., Lang, W., Zeyfang, A., et al. Multiple complications and frequent severe hypoglycaemia in ‘elderly’ and ‘old’ patients with Type 1 diabetes. Diabet Med 29 (2012), e176–e179.
36. [36] Schneider, J.A., Wilson, R.S., Bienias, J.L., Evans, D.A., Bennett, D.A., Cerebral infarctions and the likelihood of dementia from Alzheimer disease pathology. Neurology 62 (2004), 1148–1155.
37. [37] Erten-Lyons, D., Woltjer, R.L., Dodge, H., Nixon, R., Vorobik, R., Calvert, J.F., et al. Factors associated with resistance to dementia despite high Alzheimer disease pathology. Neurology 72 (2009), 354–360.
38. [38] Montine, T.J., Phelps, C.H., Beach, T.G., Bigio, E.H., Cairns, N.J., Dickson, D.W., et al. National Institute on Aging-Alzheimer's Association guidelines for the neuropathological assessment of Alzheimer's disease: A practical approach. Acta Neuropathol 123 (2012), 1–11.
39. [39] Folstein, M., Folstein, S.E., McHugh, P.R., “Mini-Mental State”: A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12 (1975), 189–198.
40. [40] Rosen, W.G., Verbal fluency in aging and dementia. J Clin Neuropsychol 2 (1980), 135–146.
41. [41] Folsom, A.R., Rasmussen, M.L., Chambless, L.E., Howard, G., Cooper, L.S., Schmidt, M.I., et al. Prospective associations of fasting insulin, body fat distribution, and diabetes with risk of ischemic stroke: The Atherosclerosis Risk in Communities (ARIC) Study investigators. Diabetes Care 22 (1999), 1077–1083.
42. [42] MacKnight, C., Rockwood, K., Awalt, E., McDowell, I., Diabetes mellitus and the risk of dementia, Alzheimer's disease and vascular cognitive impairment in the Canadian Study of Health and Aging. Dement Geriatr Cogn Disord 14 (2002), 77–83.
43. [43] Almdal, T., Scharling, H., Jensen, J.S., Vestergaard, H., The independent effect of type 2 diabetes mellitus on ischemic heart disease, stroke, and death: A population-based study of 13,000 men and women with 20 years of follow-up. Arch Intern Med 164 (2004), 1422–1426.
44. [44] Air, E.L., Kissela, B.M., Diabetes, the metabolic syndrome, and ischemic stroke. Epidemiology and possible mechanisms. Diabetes Care 30 (2007), 3131–3140.
45. [45] Mast, H., Thompson, J.L., Lee, S., Mohr, J.P., Sacco, R.P., Hypertension and diabetes mellitus as determinants of multiple lacunar infarcts. Stroke 26 (1995), 30–33.
46. [46] Akomolafe, A., Beiser, A., Meigs, J.B., Au, R., Green, R.C., Farrer, L.A., et al. Diabetes mellitus and risk of developing Alzheimer disease. Results from the Framingham Study. Arch Neurol 63 (2006), 1551–1555.
47. [47] Yarchoan, M., Toledo, J.B., Lee, E.B., Arvanitakis, Z., Kazi, H., Han, L.Y., et al. Abnormal serine phosphorylation of insulin receptor substrate 1 is associated with tau pathology in Alzheimer's disease and tauopathies. Acta Neuropathol 128 (2014), 679–689.
48. [48] Vandal, M., White, P.J., Tremblay, C., St-Amour, I., Chevrier, G., Emond, V., et al. Insulin reverses the high-fat diet-induced increase in brain Aβ and improves memory in an animal model of Alzheimer disease. Diabetes 63 (2014), 4291–4301.