Type 2 diabetes as a risk factor for cognitive impairment: Current insights

Clinical Interventions in Aging

Volumn 9, Issue , 2014, Pages 1011-1019

  Umegaki, Hiroyuki ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Amyloid ; Blood glucose; Dementia; Insulin resistance; Small vascular disease; Tau

Indexed keywords

INSULIN;

BLOOD BRAIN BARRIER; BLOOD GLUCOSE MONITORING; CLINICAL ASSESSMENT; COGNITIVE DEFECT; DEMENTIA; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE PREDISPOSITION; GLYCEMIC CONTROL; HIGH RISK PATIENT; HUMAN; HYPERGLYCEMIA; INFLAMMATION; INSULIN RESISTANCE; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NON INSULIN DEPENDENT DIABETES MELLITUS; REVIEW; RISK FACTOR; VASCULAR DISEASE; AGED; COGNITION DISORDERS; DEMENTIA, VASCULAR; DIABETES MELLITUS, TYPE 2;

AGED; COGNITION DISORDERS; DEMENTIA, VASCULAR; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN RESISTANCE; RISK FACTORS;

EID: 84903577729     PISSN: 11769092     EISSN: 11781998     Source Type: Journal    
DOI: 10.2147/CIA.S48926     Document Type: Review

References (98)

1. Danaei G, Finucane MM, Lu Y, et al; Global Burden of Metabolic Risk Factors of Chronic Diseases Collaborating Group (Blood Glucose). National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet. 2011;378(9785):31-40.
2. Abi Khalil C, Roussel R, Mohammedi K, Danchin N, Marre M. Cause-specifc mortality in diabetes: recent changes in trend mortality. Eur J Prev Cardiol. 2012;19(3):374-381.
3. McCrimmon RJ, Ryan CM, Frier BM. Diabetes and cognitive dysfunction. Lancet. 2012;379(9833):2291-2299.
4. Stewart R, Liolitsa D. Type 2 diabetes mellitus, cognitive impairment and dementia. Diabet Med. 1999;16(2):93-112.
5. Li L, Hölscher C. Common pathological processes in Alzheimer disease and type 2 diabetes: a review. Brain Res Rev. 2007;56(2):384-402.
6. Ott A, Stolk RP, van Harskamp F, et al. Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology. 1999;53(9):1937-1942.
7. Arvanitakis Z, Wilson RS, Bienias JL, Evans DA, Bennett DA. Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function. Arch Neurol. 2004;61(5):661-666.
8. Peila R, Rodriguez BL, Launer LJ; Honolulu-Asia Aging Study. Type 2 diabetes, APOE gene, and the risk for dementia and related pathologies: The Honolulu-Asia Aging Study. Diabetes. 2002;51(4):1256-1262.
9. Ohara T, Doi Y, Ninomiya T, et al. Glucose tolerance status and risk of dementia in the community: the Hisayama study. Neurology. 2011; 77(12): 1126-1134.
10. Cheng G, Huang C, Deng H, Wang H. Diabetes as a risk factor for dementia and mild cognitive impairment: a meta-analysis of longitudinal studies. Intern Med J. 2012;42(5):484-491.
11. McKhann GM, Knopman DS, Chertkow H, et al. The diagnosis of dementia due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. 2011;7(3):263-269.
12. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed. Washington, DC: American Psychiatric Association; 2000.
13. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of the Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology. 1984;34(7):939-944.
14. Jellinger KA. Prevalence and impact of cerebrovascular lesions in Alzheimer and lewy body diseases. Neurodegener Dis. 2010;7(1/3): 112-115.
15. Schneider JA, Arvanitakis Z, Bang W, Bennett DA. Mixed brain pathologies account for most dementia cases in community-dwelling older persons. Neurology. 2007;69(24):2197-2204.
16. Lee SW, Clemenson GD, Gage FH. New neurons in an aged brain. Behav Brain Res. 2012;227(2):497-507.
17. Lang BT, Yan Y, Dempsey RJ, Vemuganti R. Impaired neurogenesis in adult type-2 diabetic rats. Brain Res. 2009;1258:25-33.
18. Machida M, Fujimaki S, Hidaka R, Asashima M, Kuwabara T. The insulin regulatory network in adult hippocampus and pancreatic endocrine system. Stem Cells Int. 2012;2012:959737.
19. Farrall AJ, Wardlaw JM. Blood-brain barrier: ageing and microvascu-lar disease - systematic review and meta-analysis. Neurobiol Aging. 2009;30(3):337-352.
20. Kalaria RN. Cerebral vessels in ageing and Alzheimer's disease. Pharmacol Ther. 1996;72(3):193-214.
21. Bell RD, Zlokovic BV. Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol. 2009;118(1): 103-113.
22. Iadecola C, Nedergaard M. Glial regulation of the cerebral microvas-culature. Nat Neurosci. 2007;10(11):1369-1376.
23. Mooradian AD. Central nervous system complications of diabetes mellitus - a perspective from the blood-brain barrier. Brain Res Brain Res Rev. 1997;23(3):210-218.
24. Kerti L, Witte AV, Winkler A, Grittner U, Rujescu D, Flöel A. Higher glucose levels associated with lower memory and reduced hippocampal microstructure. Neurology. 2013;81(20):1746-1752.
25. Crane PK, Walker R, Hubbard RA, et al. Glucose levels and risk of dementia. N Engl J Med. 2013;369(6):540-548.
26. Yamagishi S, Ueda S, Okuda S. Food-derived advanced glycation end products (AGEs): a novel therapeutic target for various disorders. Curr Pharm Des. 2007;13(27):2832-2836.
27. Valente T, Gella A, Fernàndez-Busquets X, Unzeta M, Durany N. Immunohistochemical analysis of human brain suggests pathological synergism of Alzheimer's disease and diabetes mellitus. Neurobiol Dis. 2010;37(1):67-76.
28. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8(1): 57-69.
29. Evans JL, Goldfne ID, Maddux BA, Grodsky GM. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev. 2002;23(5):599-622.
30. Moreira PI, Santos MS, Seiça R, Oliveira CR. Brain mitochondrial dysfunction as a link between Alzheimer's disease and diabetes. J Neurol Sci. 2007;257(1/2):206-214.
31. Badawi A, Klip A, Haddad P, et al. Type 2 diabetes mellitus and infam-mation: Prospects for biomarkers of risk and nutritional intervention. Diabetes Metab Syndr Obes. 2010;3:173-186.
32. Akiyama H, Barger S, Barnum S, et al. Infammation and Alzheimer's disease. Neurobiol Aging. 2000;21(3):383-421.
33. Zhao WQ, Townsend M. Insulin resistance and amyloidogenesis as common molecular foundation for type 2 diabetes and Alzheimer's disease. Biochim Biophys Acta. 2009;1792(5):482-496.
34. Watson GS, Craft S. The role of insulin resistance in the pathogen-esis of Alzheimer's disease: implications for treatment. CNS Drugs. 2003;17(1):27-45.
35. Davis SN, Granner DK. Insulin, oral hypoglycemic agents, and the pharmacology of the endocrine pancreas. In: Hardman JG, Gilman AG, Limbird LE. Goodman and Gilman's the Pharmacological Basis of Therapeutics. 9th ed., New York: McGraw-Hill; 1996:1487-1517.
36. Woods SC, Seeley RJ, Baskin DG, Schwartz MW. Insulin and the blood-brain barrier. Curr Pharm Des. 2003;9(10):795-800.
37. Havrankova J, Roth J, Brownstein M. Insulin receptors are widely distributed in the central nervous system of the rat. Nature. 1978;272(5656): 827-829.
38. Freychet P. Insulin receptors and insulin action in the nervous system. Diab Metab Res Rev. 2000;16(6):390-392.
39. Rivera EJ, Goldin A, Fulmer N, Tavares R, Wands JR, de la Monte SM. Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine. J Alzheimers Dis. 2005;8(3):247-268.
40. Zhao L, Teter B, Morihara T, et al. Insulin-degrading enzyme as a downstream target of insulin receptor signaling cascade: implications for Alzheimer's disease intervention. J Neurosci. 2004;24(49): 11120-11126.
41. Ho L, Qin W, Pompl PN, et al. Diet-induced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer's disease. FASEB J. 2004;18(7):902-904.
42. Umegaki H. Pathophysiology of cognitive dysfunction in older people with type 2 diabetes: vascular changes or neurodegeneration? Age Ageing. 2010;39(1):8-10.
43. Schubert M, Brazil DP, Burks DJ, et al. Insulin receptor substrate-2 defciency impairs brain growth and promotes tau phosphorylation. J Neurosci. 2003;23(18):7084-7092.
44. Talbot K, Wang HY, Kazi H, 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. 2012;122(4): 1316-1338.
45. Bomfm TR, Forny-Germano L, Sathler LB, 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. 2012; 122(4):1339-1353.
46. Benedict C, Hallschmid M, Hatke A, et al. Intranasal insulin improves memory in humans. Psychoneuroendocrinology. 2004;29(10): 1326-1334.
47. de Zeeuw D, Parving HH, Henning RH. Microalbuminuria as an early marker for cardiovascular disease. J Am Soc Nephrol. 2006;17(8): 2100-2105.
48. de Bresser J, Reijmer YD, van den Berg E, et al; Utrecht Diabetic Encephalopathy Study Group. Microvascular determinants of cognitive decline and brain volume change in elderly patients with type 2 diabetes. Dement Geriatr Cogn Disord. 2010;30(5):381-386.
49. Kawamura T, Umemura T, Umegaki H, et al. Effect of renal impairment on cognitive function during a 3-year follow-up in elderly patients with type 2 diabetes: association with microinfammation. J Diabetes Investig. Epub 2014 Feb 4.
50. Umegaki H, Iimuro S, Shinozaki T, et al; Japanese Elderly Diabetes Intervention Trial Study Group. Risk factors associated with cognitive decline in the elderly with type 2 diabetes: baseline data analysis of the Japanese Elderly Diabetes Intervention Trial. Geriatr Gerontol Int. 2012;12 Suppl 1:103-109.
51. Umemura T, Kawamura T, Umegaki H, et al. Association of chronic kidney disease and cerebral small vessel disease with cognitive impairment in elderly patients with type 2 diabetes. Dement Geriatr Cogn Dis Extra. 2013;3(1):212-222.
52. Dalkara T, Gursoy-Ozdemir Y, Yemisci M. Brain microvascular peri-cytes in health and disease. Acta Neuropathol. 2011;122(1):1-9.
53. Weller RO, Massey A, Kuo YM, Roher AE. Cerebral amyloid angiopathy: accumulation of A beta in interstitial fuid drainage pathways in Alzheimer's disease. Ann N Y Acad Sci. 2000;903:110-117.
54. van Harten B, de Leeuw FE, Weinstein HC, Scheltens P, Biessels GJ. Brain imaging in patients with diabetes: a systematic review. Diabetes Care. 2006;29(11):2539-2548.
55. Manschot SM, Brands AM, van der Grond J, et al; Utrecht Diabetic Encephalopathy Study Group. Brain magnetic resonance imaging correlates of impaired cognition in patients with type 2 diabetes. Diabetes. 2006;55(4):1106-1113.
56. Korf ES, van Straaten EC, de Leeuw FE, et al; LADIS Study Group. Diabetes mellitus, hypertension and medial temporal lobe atrophy: the LADIS study. Diabet Med. 2007;24(2):166-171.
57. Last D, Alsop DC, Abduljalil AM, et al. Global and regional effects of type 2 diabetes on brain tissue volumes and cerebral vasoreactivity. Diabetes Care. 2007;30(5):1193-1199.
58. Gold SM, Dziobek I, Sweat V, et al. Hippocampal damage and memory impairments as possible early brain complications of type 2 diabetes. Diabetologia. 2007;50(4):711-719.
59. Bruehl H, Wolf OT, Sweat V, Tirsi A, Richardson S, Convit A. Modifers of cognitive function and brain structure in middle-aged and elderly individuals with type 2 diabetes mellitus. Brain Res. 2009;1280: 186-194.
60. Burns JM, Donnelly JE, Anderson HS, et al. Peripheral insulin and brain structure in early Alzheimer disease. Neurology. 2007;69(11): 1094-1104.
61. Burns JM, Honea RA, Vidoni ED, Hutfes LJ, Brooks WM, Swerdlow RH. Insulin is differentially related to cognitive decline and atrophy in Alzheimer's disease and aging. Biochim Biophys Acta. 2012;1822(3): 333-339.
62. den Heijer T, Vermeer SE, van Dijk EJ, et al. Type 2 diabetes and atrophy of medial temporal lobe structures on brain MRI. Diabetologia. 2003;46(12):1604-1610.
63. Willette AA, Xu G, Johnson SC, et al. Insulin resistance, brain atrophy, and cognitive performance in late middle-aged adults. Diabetes Care. 2013;36(2):443-449.
64. Moran C, Phan TG, Chen J, et al. Brain atrophy in type 2 diabetes: regional distribution and infuence on cognition. Diabetes Care. 2013; 36(12):4036-4042.
65. Baker LD, Cross DJ, Minoshima S, Belongia D, Watson GS, Craft S. Insulin resistance and Alzheimer-like reductions in regional cerebral glucose metabolism for cognitively normal adults with prediabetes or early type 2 diabetes. Arch Neurol. 2011;68(1):51-57.
66. Schrijvers EM, Witteman JC, Sijbrands EJ, Hofman A, Koudstaal PJ, Breteler MM. Insulin metabolism and the risk of Alzheimer disease: The Rotterdam Study. Neurology. 2010;75(22):1982-1987.
67. Matsuzaki T, Sasaki K, Tanizaki Y, et al. Insulin resistance is associated with the pathology of Alzheimer disease: the Hisayama study. Neurology. 2010;75(9):764-770.
68. Beeri MS, Silverman JM, Davis KL, et al. Type 2 diabetes is negatively associated with Alzheimer's disease neuropathology. J Gerontol A Biol Sci Med Sci. 2005;60(4):471-475.
69. Arvanitakis Z, Schneider JA, Wilson RS, et al. Diabetes is related to cerebral infarction but not to AD pathology in older persons. Neurology. 2006;67(11):1960-1965.
70. Thambisetty M, Jeffrey Metter E, Yang A, et al. Glucose intolerance, insulin resistance, and pathological features of Alzheimer disease in the Baltimore Longitudinal Study of Aging. JAMA Neurol. 2013;70(9):1167-1172.
71. Tomita N, Furukawa K, Okamura N, et al. Brain accumulation of amyloid β protein visualized by positron emission tomography and BF-227 in Alzheimer's disease patients with or without diabetes mel-litus. Geriatr Gerontol Int. 2013;13(1):215-221.
72. Strittmatter WJ, Roses AD. Apolipoprotein E and Alzheimer disease. Proc Natl Acad Sci U S A. 1995;92(11):4725-4727.
73. Dore GA, Elias MF, Robbins MA, Elias PK, Nagy Z. Presence of the APOE epsilon4 allele modifes the relationship between type 2 diabetes and cognitive performance: the Maine-Syracuse Study. Diabetologia. 2009;52(12):2551-2560.
74. Irie F, Fitzpatrick AL, Lopez OL, et al. Enhanced risk for Alzheimer disease in persons with type 2 diabetes and APOE epsilon4: the Cardiovascular Health Study Cognition Study. Arch Neurol. 2008;65(1):89-93.
75. Luitse MJ, Biessels GJ, Rutten GE, Kappelle LJ. Diabetes, hyperglycae-mia, and acute ischaemic stroke. Lancet Neurol. 2012;11(3):261-271.
76. Reijmer YD, Leemans A, Brundel M, Kappelle LJ, Biessels GJ; Utrecht Vascular Cognitive Impairment Study Group. Disruption of the cerebral white matter network is related to slowing of information processing speed in patients with type 2 diabetes. Diabetes. 2013;62(6):2112-2115.
77. Reijmer YD, Brundel M, de Bresser J, Kappelle LJ, Leemans A, Biessels GJ; Utrecht Vascular Cognitive Impairment Study Group. Microstructural white matter abnormalities and cognitive functioning in type 2 diabetes: a diffusion tensor imaging study. Diabetes Care. 2013;36(1):137-144.
78. Cukierman-Yaffe T, Gerstein HC, Williamson JD, et al; Action to Control Cardiovascular Risk in Diabetes-Memory in Diabetes (ACCORD-MIND) Investigators. Relationship between baseline glycemic control and cognitive function in individuals with type 2 diabetes and other cardiovascular risk factors: the action to control cardiovascular risk in diabetes-memory in diabetes (ACCORD-MIND) trial. Diabetes Care. 2009;32(2):221-226.
79. Maggi S, Limongi F, Noale M, et al; ILSA Study Group. Diabetes as a risk factor for cognitive decline in older patients. Dement Geriatr Cogn Disord. 2009;27(1):24-33.
80. Peters R, Beckett N, Forette F, et al; HYVET investigators. Incident dementia and blood pressure lowering in the Hypertension in the Very Elderly Trial cognitive function assessment (HYVET-COG): a double-blind, placebo controlled trial. Lancet Neurol. 2008;7(8):683-689.
81. Umegaki H, Kawamura T, Mogi N, Umemura T, Kanai A, Sano T. Glucose control levels, ischaemic brain lesions, and hyperinsulinaemia were associated with cognitive dysfunction in diabetic elderly. Age Ageing. 2008;37(4):458-461.
82. Launer LJ, Miller ME, Williamson JD, et al; ACCORD MIND investigators. Effects of intensive glucose lowering on brain structure and function in people with type 2 diabetes (ACCORD MIND): a randomised open-label substudy. Lancet Neurol. 2011;10(11):969-977.
83. Luchsinger JA, Palmas W, Teresi JA, et al. Improved diabetes control in the elderly delays global cognitive decline. J Nutr Health Aging. 2011;15(6):445-449.
84. Ikonomovic MD, Klunk WE, Abrahamson EE, et al. Post-mortem correlates of in vivo PiB-PET amyloid imaging in a typical case of Alzheimer's disease. Brain. 2008;131(Pt 6):1630-1645.
85. van den Berg E, Reijmer YD, de Bresser J, Kessels RP, Kappelle LJ, Biessels GJ, Utrecht Diabetic Encephalopathy Study Group. A 4 year follow-up study of cognitive functioning in patients with type 2 diabetes mellitus. Diabetologia. 2010;53(1):58-65.
86. Shorr RI, de Rekeneire N, Resnick HE, et al. Glycemia and cognitive function in older adults using glucose-lowering drugs. J Nutr Health Aging. 2006;10(4):297-301.
87. Whitmer RA, Karter AJ, Yaffe K, Quesenberry CP, Selby JV. Hypo-glycemic episodes and risk of dementia in older patients with type 2 diabetes mellitus. JAMA. 2009;301(15):1565-1572.
88. Novak V, Abduljalil AM, Novak P, Robitaille PM. High-resolution ultrahigh-feld MRI of stroke. Magn Reson Imaging. 2005;23(4): 539-548.
89. Kodl CT, Franc DT, Rao JP, et al. Diffusion tensor imaging identifes defcits in white matter microstructure in subjects with type 1 diabetes that correlate with reduced neurocognitive function. Diabetes. 2008;57(11):3083-3089.
90. Zetterberg LO, Wahlund K, Blennow. Cerebrospinal fuid markers for prediction of Alzheimer's disease. Neurosci Lett. 2003;352(1):67-69.
91. Hansson H, Zetterberg P, Buchhave E, Londos E, Blennow K, Minthon L. Association between CSF biomarkers and incipient Alzheimer's disease in patients with mild cognitive impairment: a follow-up study. Lancet Neurol. 2006;5(3):228-234.
92. Ewers M, Buerger K, Teipel SJ, et al. Multicenter assessment of CSF-phosphorylated tau for the prediction of conversion of MCI. Neurology. 2007;69(24):2205-2212.
93. Schiöth HB, Craft S, Brooks SJ, Frey WH, Benedict C. Brain insulin signaling and Alzheimer's disease: current evidence and future directions. Mol Neurobiol. 2012;46(1):4-10.
94. McIntyre RS, Powell AM, Kaidanovich-Beilin O, et al. The neuroprotec-tive effects of GLP-1: possible treatments for cognitive defcits in individuals with mood disorders. Behav Brain Res. 2013;237:164-171.
95. Gouw AA, van der Flier WM, Fazekas F, et al; LADIS Study Group. Progression of white matter hyperintensities and incidence of new lacunes over a 3-year period: the Leukoaraiosis and Disability study. Stroke. 2008;39(5):1414-1420.
96. van Eersel ME, Joosten H, Gansevoort RT, Dullaart RP, Slaets JP, Izaks GJ. The interaction of age and type 2 diabetes on executive function and memory in persons aged 35 years or older. PLoS One. 2013; 8(12):e82991.
97. Joosten H, van Eersel ME, Gansevoort RT, Bilo HJ, Slaets JP, Izaks GJ. Cardiovascular risk profle and cognitive function in young, middle-aged, and elderly subjects. Stroke. 2013;44(6):1543-1549.
98. Tang J, Pei Y, Zhou G. When aging-onset diabetes is coming across with Alzheimer disease: comparable pathogenesis and therapy. Exp Gerontol. 2013;48(8):744-750.