Cognitive dysfunction in patients with type 2 diabetes

Diabetes/Metabolism Research and Reviews

Volumn 26, Issue 7, 2010, Pages 507-519

  Reijmer, Yael D ^a   van den Berg, Esther ^a,b   Ruis, Carla ^a,b   Kappelle, L Jaap ^a   Biessels, Geert Jan ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Cognitive functioning; Dementia; Diabetes mellitus; Imaging; Neuropsychological assessment; Vascular risk factors

Indexed keywords

AUTOPSY; COGNITIVE DEFECT; DEMENTIA; DEPRESSION; DIABETIC ANGIOPATHY; DIABETIC MICROANGIOPATHY; DISEASE SEVERITY; HUMAN; HYPERGLYCEMIA; HYPOGLYCEMIA; NEUROIMAGING; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; REVIEW; RISK FACTOR;

BRAIN; COGNITION DISORDERS; DEMENTIA; DEPRESSION; DIABETES MELLITUS, TYPE 2; DIABETIC ANGIOPATHIES; FEMALE; HUMANS; HYPERGLYCEMIA; HYPOGLYCEMIA; LIFE STYLE; MALE; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RISK FACTORS;

EID: 78650794280     PISSN: 15207552     EISSN: 15207560     Source Type: Journal    
DOI: 10.1002/dmrr.1112     Document Type: Review

References (167)

1. Ryan CM, Geckle MO. Circumscribed cognitive dysfunction in middle-aged adults with type 2 diabetes. Diabetes Care 2000; 23: 1486-1493.
2. Reaven GM, Thompson LW, Nahum D, Haskins E. Relationship between hyperglycemia and cognitive function in older NIDDM patients. Diabetes Care 1990; 13: 16-21.
3. Brands AMA, van den Berg E, Manschot SM, et al. Adetailed profile of cognitive dysfunction and its relation to psychological distress in patients with type 2 diabetes mellitus. J Int Neuropsychol Soc 2007; 13: 288-297.
4. van Harten B, Oosterman J, Muslimovic D, van Loon BJ, Scheltens P, Weinstein HC. Cognitive impairment and MRI correlates in the elderly patients with type 2 diabetes mellitus. Age Ageing 2007; 36: 164-170.
5. Wahlin A, Nilsson E, Fastbom J. Cognitive performance in very old diabetic persons: the impact of semantic structure, preclinical dementia, and impending death. Neuropsychology 2002; 16: 208-216.
6. van den Berg E, Kloppenborg RP, Kessels RP, Kappelle LJ, Biessels GJ. Type 2 diabetes mellitus, hypertension, dyslipidemia and obesity: a systematic comparison of their impact on cognition. Biochim Biophys Acta 2009; 1792: 470-481.
7. Haan MN, Shemanski L, Jagust WJ, Manolio TA, Kuller L. The role of APOE epsilon4 in modulating effects of other risk factors for cognitive decline in elderly persons. JAMA 1999; 282: 40-46.
8. Ruis C, Biessels GJ, Gorter KJ, van den Donk M, Kappelle LJ, Rutten GE. Cognition in the early stage of type 2 diabetes. Diabetes Care 2009; 32: 1261-1265.
9. van den Berg E, Dekker JM, Nijpels G, et al. Cognitive functioning in elderly persons with type 2 diabetes and metabolic syndrome: the Hoorn study. Dement Geriatr Cogn Disord 2008; 26: 261-269.
10. Baddeley A. Working memory. Science 1992; 255: 556-559.
11. Cerhan JR, Folsom AR, Mortimer JA, et al. Correlates of cognitive function in middle-aged adults. Gerontology 1998; 44: 95-105.
12. Elias PK, Elias MF, D'Agostino RB, et al. NIDDM and blood pressure as risk factors for poor cognitive performance. The Framingham Study. Diabetes Care 1997; 20: 1388-1395.
13. Atiea JA, Moses JL, Sinclair AJ. Neuropsychological function in older subjects with non-insulin-dependent diabetes mellitus. Diabetic Med 1995; 12: 679-685.
14. Scott RD, Kritz-Silverstein D, Barrett-Connor E, Wiederholt WC. The association of non-insulin-dependent diabetes mellitus and cognitive function in an older cohort. J Am Geriatr Soc 1998; 46: 1217-1222.
15. Cosway R, Strachan MW, Dougall A, Frier BM, Deary IJ. Cognitive function and information processing in type 2 diabetes. Diabet Med 2001; 18: 803-810.
16. Lindeman RD, Romero LJ, LaRue A, et al.Abiethniccommunity survey of cognition in participants with type 2 diabetes, impaired glucose tolerance, and normal glucose tolerance: the New Mexico Elder Health Survey. Diabetes Care 2001; 24: 1567-1572.
17. Gregg EW, Yaffe K, Cauley JA, et al.Isdiabetesassociated with cognitive impairment and cognitive decline among older women? Study of Osteoporotic Fractures Research Group. Arch Intern Med 2000; 160: 174-180.
18. Stewart R, Prince M, Mann A. Age, vascular risk, and cognitive decline in an older, British, African-Caribbean population. J Am Geriatr Soc 2003; 51: 1547-1553.
19. Hassing LB, Johansson B, Pedersen NL, Nilsson SE, Berg S, McClearn G. Type 2 diabetes mellitus and cognitive performance in a population-based sample of the oldest old: impact of comorbid dementia. Aging Neuropsy Cogn 2004; 10: 99-107.
20. Knopman D, Boland LL, Mosley T, et al. Cardiovascular risk factors and cognitive decline in middle-aged adults. Neurology 2001; 56: 42-48.
21. Fontbonne A, Berr C, Ducimetiere P, Alperovitch A. Changes in cognitive abilities over a 4-year period are unfavorably affected in elderly diabetic subjects: results of the Epidemiology of vascular aging study. Diabetes Care 2001; 24: 366-370.
22. Kanaya AM, Barrett-Connor E, Gildengorin G, Yaffe K. Change in cognitive function by glucose tolerance status in older adults: a 4-year prospective study of the Rancho Bernardo study cohort. Arch Intern Med 2004; 164: 1327-1333.
23. Yaffe K, Blackwell T, Kanaya AM, Davidowitz N, Barrett-Connor E, Krueger K. Diabetes, impaired fasting glucose, and development of cognitive impairment in older women. Neurology 2004; 63: 658-663.
24. van den Berg E, Reijmer YD, de Bresser J, Kessels RP, Kappelle LJ, Biessels GJ. A 4 year follow-up study of cognitive functioning in patients with type 2 diabetes mellitus. Diabetologia 2010; 53: 58-65.
25. Wu JH, Haan MN, Liang J, Ghosh D, Gonzalez HM, Herman WH. Impact of diabetes on cognitive function among older Latinos: a population-based cohort study. J Clin Epidemiol 2003; 56: 686-693.
26. Fischer AL, De Frias CM, Yeung SE, Dixon RA. Short-term longitudinal trends in cognitive performance in older adults with type 2 diabetes. J Clin Exp Neuropsychol 2009; 31: 809-822.
27. Amieva H, Jacqmin-Gadda H, Orgogozo JM, et al.The9year cognitive decline before dementia of the Alzheimer type: a prospective population-based study. Brain 2005; 128: 1093-1101.
28. Lopez OL, Jagust WJ, Dulberg C, et al. Risk factors for mild cognitive impairment in the Cardiovascular Health Study Cognition Study: part 2. Arch Neurol 2003; 60: 1394-1399.
29. Toro P, Schönknecht P, Schröder J. Type II diabetes in mild cognitive impairment and Alzheimer's disease: results from a prospective population-based study in Germany. J Alzheimers Dis 2009; 16: 687-691.
30. Luchsinger JA, Tang MX, 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 2001; 154: 635-641.
31. Luchsinger JA, Reitz C, Patel B, Tang MX, Manly JJ, Mayeux R. Relation of diabetes to mild cognitive impairment. Arch Neurol 2007; 64: 570-575.
32. Yaffe K, Blackwell T, Whitmer RA, Krueger K, Barrett-Connor E. Glycosylated hemoglobin level and development of mild cognitive impairment or dementia in older women. J Nutr Health Aging 2006; 10: 292-295.
33. Solfrizzi V, Panza F, Colacicco AM, et al. Vascular risk factors, incidence of MCI, and rates of progression to dementia. Neurology 2004; 63: 1882-1891.
34. Biessels GJ, Staekenborg S, Brunner E, Brayne C, Scheltens P. Risk of dementia in diabetes mellitus: a systematic review. Lancet Neurol 2006; 5: 64-74.
35. Kloppenborg RP, van den Berg E, Kappelle LJ, Biessels GJ. Diabetes and other vascular risk factors for dementia: which factor matters most? A systematic review. Eur J Pharmacol 2008; 585: 97-108.
36. Yoshitake T, Kiyohara Y, Kato I, et al. Incidence and risk factors of vascular dementia and Alzheimer's disease in a defined elderly Japanese population: the Hisayama Study. Neurology 1995; 45: 1161-1168.
37. Ott A, Stolk RP, van Harskamp F, Pols HA, Hofman A, Breteler MM. Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology 1999; 53: 1937-1942.
38. Peila R, Rodriguez BL, Launer LJ. Type 2 diabetes, APOE gene, and the risk for dementia and related pathologies: The Honolulu-Asia Aging Study. Diabetes 2002; 51: 1256-1262.
39. Xu WL, Qiu CX, Wahlin A, Winblad B, Fratiglioni L. Diabetes mellitus and risk of dementia in the Kungsholmen project: a 6-year follow-up study. Neurology 2004; 63: 1181-1186.
40. Luchsinger JA, Reitz C, Honig LS, Tang MX, Shea S, Mayeux R. Aggregation of vascular risk factors and risk of incident Alzheimer disease. Neurology 2005; 65: 545-551.
41. 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: 661-666.
42. Hassing LB, Johansson B, Nilsson SE, et al. Diabetes mellitus is a risk factor for vascular dementia, but not for Alzheimer's disease: a population-based study of the oldest old. Int Psychogeriatr 2002; 14: 239-248.
43. Jellinger KA, Attems J. Prevalence of dementia disorders in the oldest-old: an autopsy study. Acta Neuropathol 2010; 119: 421-433.
44. Vanhanen M, Koivisto K, Kuusisto J, et al. Cognitive function in an elderly population with persistent impaired glucose tolerance. Diabetes Care 1998; 21: 398-402.
45. Messier C, Tsiakas M, Gagnon M, Desrochers A, Awad N. Effect of age and glucoregulation on cognitive performance. Neurobiol Aging 2003; 24: 985-1003.
46. Young SE, Mainous AG, III. Carnemolla M. Hyperinsulinemia and cognitive decline in a middle-aged cohort. Diabetes Care 2006; 29: 2688-2693.
47. Kumari M, Marmot M. Diabetes and cognitive function in a middle-aged cohort: findings from the Whitehall II study. Neurology 2005; 65: 1597-1603.
48. Fuh JL, Wang SJ, Hwu CM, Lu SR. Glucose tolerance status and cognitive impairment in early middle-aged women. Diabet Med 2007.
49. Reaven GM. Banting lecture 1988. Role of insulin resistance in human disease. Diabetes 1988; 37: 1595-1607.
50. Dik MG, Jonker C, Comijs HC, et al. Contribution of metabolic syndrome components to cognition in older individuals. Diabetes Care 2007; 30: 2655-2660.
51. Kalmijn S, Feskens EJM, Launer LJ, Stijnen T, Kromhout D. Glucose intolerance, hyperinsulinaemia and cognitive function in a general population of elderly men. Diabetologia 1995; 38: 1096-1102.
52. Geroldi C, Frisoni GB, Paolisso G, et al. Insulin resistance in cognitive impairment: the InCHIANTI study. Arch Neurol 2005; 62: 1067-1072.
53. Kalmijn S, Foley D, White L, et al. Metabolic cardiovascular syndrome and risk of dementia in Japanese-American elderly men. The Honolulu-Asia aging study. Arterioscler Thromb Vasc Biol 2000; 20: 2255-2260.
54. Luchsinger JA, Tang MX, Shea S, Mayeux R. Hyperinsulinemia and risk of Alzheimer disease. Neurology 2004; 63: 1187-1192.
55. Anderson RJ, Freedland KE, Clouse RE, Lustman PJ. The prevalence of comorbid depression in adults with diabetes: a meta-analysis. Diabetes Care 2001; 24: 1069-1078.
56. Umegaki H, Iimuro S, Kaneko T, et al. Factors associated with lower Mini Mental State Examination scores in elderly Japanese diabetes mellitus patients. Neurobiol Aging 2008; 29: 1022-1026.
57. Krabbe KS, Nielsen AR, Krogh-Madsen R, et al. Brain-derived neurotrophic factor (BDNF) and type 2 diabetes. Diabetologia 2007; 50: 431-438.
58. Baldwin RC, O'Brien J. Vascular basis of late-onset depressive disorder. Br J Psychiatry 2002; 180: 157-160.
59. Bruce DG, Casey G, Davis WA, et al. Vascular depression in older people with diabetes. Diabetologia 2006; 49: 2828-2836.
60. Knol MJ, Twisk JWR, Beekman ATF, Heine RJ, Snoek FJ, Pouwer F. Depression as a risk factor for the onset of type 2 diabetes mellitus. A meta-analysis. Diabetologia 2006; 49: 837-845.
61. Ryan CM, Geckle M. Why is learning and memory dysfunction in Type 2 diabetes limited to older adults?, Diabetes Metab Res Rev 2000; 16: 308-315.
62. Roriz-Filho S, Sá-Roriz TM, Rosset I, et al. (Pre)diabetes, brain aging, and cognition. Biochim Biophys Acta -Mol Basis Dis 2009; 1792: 432-443.
63. Biessels GJ, Deary IJ, Ryan CM. Cognition and diabetes: a lifespan perspective. Lancet Neurol 2008; 7: 184-190.
64. Okereke OI, Kang JH, Cook NR, et al. Type 2 diabetes mellitus and cognitive decline in two large cohorts of community-dwelling older adults. J Am Geriatr Soc 2008; 56: 1028-1036.
65. Maggi S, Limongi F, Noale M, et al.Diabetesasariskfactorfor cognitive decline in older patients. Dement Geriatr Cogn Disord 2009; 27: 24-33.
66. Robbins JM, Vaccarino V, Zhang H, Kasl SV. Socioeconomic status and type 2 diabetes in African American and non-Hispanic White women and men: Evidence from the Third National Health and Nutrition Examination Survey. Am J Public Health 2001; 91: 76-83.
67. Harris MI, Flegal KM, Cowie CC, et al. Prevalence of diabetes, impaired fasting glucose, and impaired glucose tolerance in U.S. adults: The Third National Health and Nutrition Examination Survey, 1988-1994. Diabetes Care 1998; 21: 518-524.
68. Miles TP, Froehlich TE, Bogardus J, Inouye SK. Dementia and race: Are there differences between African Americans and Caucasians? J Am Geriatr Soc 2001; 49: 477-484.
69. Nicolucci A, Cucinotta D, Squatrito S, et al. Clinical and socioeconomic correlates of quality of life and treatment satisfaction in patients with type 2 diabetes. Nutr Metab Cardiovasc Dis 2009; 19: 45-53.
70. Egede LE, Zheng D. Modifiable cardiovascular risk factors in adults with diabetes: prevalence and missed opportunities for physician counseling. Arch Int Med 2002; 162: 427-433.
71. Berry EM. Dietary fatty acids in the management of diabetes mellitus. Am J Clin Nutr 1997; 66.
72. Launer LJ, Andersen K, Dewey ME, et al. Rates and risk factors for dementia and Alzheimer's disease: results from EURODEM pooled analyses. EURODEM Incidence Research Group and Work Groups. European Studies of Dementia. Neurology 1999; 52: 78-84.
73. Petot GJ, Friedland RP. Lipids, diet and Alzheimer disease: an extended summary. J Neurol Sci 2004; 226: 31-33.
74. Singh-Manoux A, Hillsdon M, Brunner E, Marmot M. Effects of physical activity on cognitive functioning in middle age: evidence from the whitehall II prospective Cohort study. Am J Public Health 2005; 95: 2252-2258.
75. Brands AMA, Biessels GJ, De Haan EHF, Kappelle LJ, Kessels RPC. The effects of Type 1 diabetes on cognitive performance: a meta-analysis. Diabetes Care 2005; 28: 726-735.
76. Gustafson D. A life course of adiposity and dementia. Eur J Pharmacol 2008; 585: 163-175.
77. Hassing LB, Hofer SM, Nilsson SE, et al. Comorbid type 2 diabetes mellitus and hypertension exacerbates cognitive decline: evidence from a longitudinal study. Age Ageing 2004; 33: 355-361.
78. Ferguson SC, Blane A, Perros P, et al. Cognitive ability and brain structure in type 1 diabetes: relation to microangiopathy and preceding severe hypoglycemia. Diabetes 2003; 52: 149-156.
79. Manschot SM, Brands AM, van der Grond J, et al. Brain magnetic resonance imaging correlates of impaired cognition in patients with type 2 diabetes. Diabetes 2006; 55: 1106-1113.
80. Munshi M, Grande L, Hayes M, et al. Cognitivedysfunctionis associated with poor diabetes control in older adults. Diabetes Care 2006; 29: 1794-1799.
81. 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: 711-719.
82. Ebady SA, Arami MA, Shafigh MH. Investigation on the relationship between diabetes mellitus type 2 and cognitive impairment. Diabetes Res Clin Pract 2008; 82: 305-309.
83. Cukierman-Yaffe T, Gerstein HC, Williamson JD, et al.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: 221-226.
84. Worrall GJ, Chaulk PC, Moulton N. Cognitive function and glycosylated hemoglobin in older patients with type II diabetes. J Diabetes Complicat 1996; 10: 320-324.
85. Lowe LO, Tranel D, Wallace RB, Welty TK. TypeIIdiabetes and cognitive function. Diabetes Care 1994; 17: 891-896.
86. Logroscino G, Kang JH, Grodstein F. Prospective study of type 2 diabetes and cognitive decline in women aged 70-81 years. BMJ 2004; 328: 548.
87. Cox DJ, Kovatchev BP, Gonder-Frederick LA, et al.Relationships between hyperglycemia and cognitive performance among adults with type 1 and type 2 diabetes. Diabetes Care 2005; 28: 71-77.
88. Xu WL, Von Strauss E, Qiu CX, Winblad B, Fratiglioni L. Uncontrolled diabetes increases the risk of Alzheimer's disease: a population-based cohort study. Diabetologia 2009; 52: 1031-1039.
89. Bruce DG, Davis WA, Casey GP, et al. Predictors of cognitive impairment and dementia in older people with diabetes. Diabetologia 2008; 51: 241-248.
90. Henderson JN, Allen KV, Deary IJ, Frier BM. Hypoglycaemia in insulin-treated Type 2 diabetes: frequency, symptoms and impaired awareness. Diabet Med 2003; 20: 1016-1021.
91. Heller SR, Choudhary P, Davies C, et al. Risk of hypoglycaemia in types 1 and 2 diabetes: Effects of treatment modalities and their duration. Diabetologia 2007; 50: 1140-1147.
92. Deary IJ. Symptoms of hypoglycaemia and effects on mental performance and emotions. In Hypoglycaemia in Clinical Diabetes, (2nd edn), Frier BM, Fisher M (eds). John Wiley & Sons: Chichester, 2007; 25.
93. Warren RE, Frier BM. Hypoglycaemia and cognitive function. Diabetes Obes Metab 2005; 7: 493-503.
94. Biessels GJ. Hypoglycemia and dementia in type 2 diabetes: chick or egg? Nat Rev Endocrinol 2009; 5: 532-534.
95. Whitmer RA, Karter AJ, Yaffe K, Quesenberry J, Selby JV. Hypoglycemic episodes and risk of dementia in older patients with type 2 diabetes mellitus. J Am Med Assoc 2009; 301: 1565-1572.
96. Bruce DG, Davis WA, Casey GP, et al. Severe hypoglycaemia and cognitive impairment in older patients with diabetes: The Fremantle Diabetes Study. Diabetologia 2009; 52: 1808-1815.
97. The Diabetes Control and Complications Trial Research Group Long-term effect of diabetes and its treatment on cognitive function. N Engl J Med 2007; 356: 1842-1852.
98. Manschot SM, Biessels GJ, de Valk HW, et al. Metabolic and vascular determinants of impaired cognitive performance and abnormalities on brain magnetic resonance imaging in patients with type 2 diabetes. Diabetologia 2007; 50: 2388-2397.
99. van den Berg E, Dekker JM, Nijpels G, et al. Blood pressure levels in pre-diabetic stages are associated with worse cognitive functioning in patients with type 2 diabetes. Diabetes Metab Res Rev 2009; 25: 657-664.
100. Bruehl H, Wolf OT, Sweat V, Tirsi A, Richardson S, Convit A. Modifiers of cognitive function and brain structure in middleaged and elderly individuals with type 2 diabetes mellitus. Brain Res 2009; 1280: 186-194.
101. Skoog I, Lernfelt B, Landahl S, et al. 15-year longitudinal study of blood pressure and dementia. Lancet 1996; 347: 1141-1145.
102. Longstreth WT, Jr. Bernick C, Manolio TA, Bryan N, Jungreis CA, Price TR. Lacunar infarcts defined by magnetic resonance imaging of 3660 elderly people: the Cardiovascular Health Study. Arch Neurol 1998; 55: 1217-1225.
103. Korf ES, van Straaten EC, de Leeuw FE, et al. Diabetes mellitus, hypertension and medial temporal lobe atrophy: the LADIS study. Diabet Med 2007; 24: 166-171.
104. Ryan CM, Geckle MO, Orchard TJ. Cognitive efficiency declines over time in adults with Type 1 diabetes: effects of micro-and macrovascular complications. Diabetologia 2003; 46: 940-948.
105. Wessels AM, Rombouts SA, Remijnse PL, et al.Cognitiveperformance in type 1 diabetes patients is associated with cerebral white matter volume. Diabetologia 2007; 50: 1763-1769.
106. De Luis DA, Fernandez N, Arranz M, Aller R, Izaola O. Total homocysteine and cognitive deterioration in people with type 2diabetes.Diabetes Res Clin Pract 2002; 55: 185-190.
107. Bruce DG, Davis WA, Casey GP, et al. Predictors of cognitive decline in older people with diabetes. Diabetes Care 2008; 31: 2103-2107.
108. Ding J, Patton N, Deary IJ, et al. Retinal microvascular abnormalities and cognitive dysfunction: A systematic review. Br J Ophthalmol 2008; 92: 1017-1025.
109. Barzilay JI, Fitzpatrick AL, Luchsinger J, et al. Albuminuria and dementia in the elderly: a Community study. Am J Kidney Dis 2008; 52: 216-226.
110. Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA 2002; 287: 2570-2581.
111. Mosley TH, Jr Knopman DS, Catellier DJ, et al. Cerebral MRI findings and cognitive functioning: the Atherosclerosis Risk in Communities study. Neurology 2005; 64: 2056-2062.
112. van den Berg E, de Craen AJ, Biessels GJ, Gussekloo J, Westendorp RG. The impact of diabetes mellitus on cognitive decline in the oldest of the old: a prospective population-based study. Diabetologia 2006; 49: 2015-2023.
113. Tiehuis AM, Mali WP, van Raamt AF, et al. Cognitive dysfunction and its clinical and radiological determinants in patients with symptomatic arterial disease and diabetes. J Neurol Sci 2009; 283: 170-174.
114. Slooter AJ, Tang MX, van Duijn CM, et al. Apolipoprotein E epsilon4 and the risk of dementia with stroke. A populationbased investigation. JAMA 1997; 277: 818-821.
115. Blair CK, Folsom AR, Knopman DS, Bray MS, Mosley TH, Boerwinkle E. APOE genotype and cognitive decline in a middle-aged cohort. Neurology 2005; 64: 268-276.
116. Irie F, Fitzpatrick AL, Lopez OL, et al.Enhancedriskfor Alzheimer disease in persons with type 2 diabetes and APOE epsilon4: the Cardiovascular Health Study Cognition Study. Arch Neurol 2008; 65: 89-93.
117. Dore GA, Elias MF, Robbins MA, Elias PK, Nagy Z. Presence of the APOEÎ(4 allele modifies the relationship between type 2 diabetes and cognitive performance: The Maine-Syracuse Study. Diabetologia 2009; 52: 2551-2560.
118. Qiu WQ, Folstein MF. Insulin, insulin-degrading enzyme and amyloid-beta peptide in Alzheimer's disease: review and hypothesis. Neurobiol Aging 2006; 27: 190-198.
119. Edland SD, Wavrant-De-Vriese F, Compton D, et al.Insulin degrading enzyme (IDE) genetic variants and risk of Alzheimer's disease: evidence of effect modification by apolipoprotein E (APOE). Neurosci Lett 2003; 345: 21-24.
120. Edland SD. Insulin-degrading enzyme, apolipoprotein E, and Alzheimer's disease. J Mol Neurosci 2004; 23: 213-217.
121. Gispen WH, Biessels GJ. Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci 2000; 23: 542-549.
122. Li L, Holscher C. Common pathological processes in Alzheimer disease and type 2 diabetes: a review. Brain Res Rev 2007; 56: 384-402.
123. Sima AAF, Kamiya H, Li ZG. Insulin, C-peptide, hyperglycemia, and central nervous system complications in diabetes. Eur J Pharmacol 2004; 490: 187-197.
124. Craft S, Watson GS. Insulin and neurodegenerative disease: shared and specific mechanisms. Lancet Neurol 2004; 3: 169-178.
125. Stranahan AM, Arumugam TV, Cutler RG, Lee K, Egan JM, Mattson MP. Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci 2008; 11: 309-317.
126. Reagan LP, Grillo CA, Piroli GG. The As and Ds of stress: metabolic, morphological and behavioral consequences. Eur J Pharmacol 2008; 585: 64-75.
127. Vermeer SE, Koudstaal PJ, Oudkerk M, Hofman A, Breteler MM. Prevalence and risk factors of silent brain infarcts in the populationbased Rotterdam Scan Study. Stroke 2002; 33: 21-25.
128. 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: 2539-2548.
129. Schmidt R, Launer LJ, Nilsson LG, et al. Magnetic resonance imaging of the brain in diabetes: the Cardiovascular Determinants of Dementia (CASCADE) Study. Diabetes 2004; 53: 687-692.
130. 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: 1604-1610.
131. Longstreth WT, Jr. Manolio TA, Arnold A, et al. Clinical correlates of white matter findings on cranial magnetic resonance imaging of 3301 elderly people. The Cardiovascular Health Study. Stroke 1996; 27: 1274-1282.
132. Jongen C, van der GJ, Kappelle LJ, Biessels GJ, Viergever MA, Pluim JP. Automated measurement of brain and white matter lesion volume in type 2 diabetes mellitus. Diabetologia 2007; 50: 1509-1516.
133. van Harten B, Oosterman JM, Potter van Loon BJ, Scheltens P, Weinstein HC. Brain lesions on MRI in elderly patients with type 2 diabetes mellitus. Eur Neurol 2007; 57: 70-74.
134. 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: 1193-1199.
135. Gouw AA, van der Flier WM, Fazekas F, et al. Progression of white matter hyperintensities and incidence of new lacunes over a 3-year period. The Leukoaraiosis and Disability Study. Stroke 2008; 39: 1414-1420.
136. Cordonnier C, Al-Shahi SR, Wardlaw J. Spontaneous brain microbleeds: systematic review, subgroup analyses and standards for study design and reporting. Brain 2007; 130: 1988-2003.
137. Jongen C, Biessels GJ. Structural brain imaging in diabetes: a methodological perspective. Eur J Pharmacol 2008; 585: 208-218.
138. Korf ES, White LR, Scheltens P, Launer LJ. Brain aging in very old men with type 2 diabetes: the Honolulu-Asia Aging Study. Diabetes Care 2006; 29: 2268-2274.
139. Brundel M, van den Heuvel M, de Bresser J, Kappelle LJ, Biessels GJ. on behalf of the Utrecht Diabetic Encephalopathy Study Group. Cerebral cortical thickness in patients with type 2diabetes.J Neurol Sci 2010; In Press.
140. Kumar A, Haroon E, Darwin C, et al. Gray matter prefrontal changes in type 2 diabetes detected using MRI. J Magn Reson Imaging 2008; 27: 14-19.
141. Akisaki T, Sakurai T, Takata T, et al.Cognitivedysfunction associates with white matter hyperintensities and subcortical atrophy on magnetic resonance imaging of the elderly diabetes mellitus Japanese elderly diabetes intervention trial (J-EDIT). Diabetes Metab Res Rev 2006; 22: 376-384.
142. Arvanitakis Z, Schneider JA, Wilson RS, et al.Diabetesis related to cerebral infarction but not to AD pathology in older persons. Neurology 2006; 67: 1960-1965.
143. 2-Amyloid deposition in brains of subjects with diabetes. Neuropathol Appl Neurobiol 2009; 35: 60-68.
144. Johnson PC, Brenedel K, Meezan E. Thickened cerebral cortical capillary basement membranes in diabetics. Arch Pathol Lab Med 1982; 106: 214-217.
145. Nelson PT, Smith CD, Abner EA, et al. Human cerebral neuropathology of Type 2 diabetes mellitus. Biochim Biophys Acta -Mol Basis Dis 2009; 1792: 454-469.
146. Kalaria RN, Kenny RA, Ballard CG, Perry R, Ince P, Polvikoski T. Towards defining the neuropathological substrates of vascular dementia. J Neurol Sci 2004; 226: 75-80.
147. Kovari E, Gold G, Herrmann FR, et al. Cortical microinfarcts and demyelination affect cognition in cases at high risk for dementia. Neurology 2007; 68: 927-931.
148. Sonnen JA, Larson EB, Crane PK, et al. Pathological correlates of dementia in a longitudinal, population-based sample of aging. Ann Neurol 2007; 62: 406-413.
149. Heitner J, Dickson D. Diabetics do not have increased Alzheimer-type pathology compared with age-matched control subjects. A retrospective postmortem immunocytochemical and histofluorescent study. Neurology 1997; 49: 1306-1311.
150. Schnaider Beeri M, Silverman JM, Davis KL, et al. Type2 diabetes is negatively associated with Alzheimer's disease neuropathology. J Gerontol A Biol Sci Med Sci 2005; 60: 471-475.
151. Messier C, Gagnon M. Cognitive decline associated with dementia and type 2 diabetes: the interplay of risk factors. Diabetologia 2009; 52: 2471-2474.
152. Gradman TJ, Laws A, Thompson LW, Reaven GM. Verbal learning and/or memory improves with glycemic control in older subjects with non-insulin-dependent diabetes mellitus. J Am Geriatr Soc 1993; 41: 1305-1312.
153. Meneilly GS, Cheung E, Tessier D, Yakura C, Tuokko H. The effect of improved glycemic control on cognitive functions in the elderly patient with diabetes. J Gerontol 1993; 48: M117-M121.
154. Naor M, Steingruber HJ, Westhoff K, Schottenfeld-Naor Y, Gries AF. Cognitive function in elderly non-insulin-dependent diabetic patients before and after inpatient treatment for metabolic control. J Diabetes Complicat 1997; 11: 40-46.
155. Hewer W, Mussell M, Rist F, Kulzer B, Bergis K. Short-term effects of improved glycemic control on cognitive function in patients with type 2 diabetes. Gerontology 2003; 49: 86-92.
156. Ryan CM, Freed MI, Rood JA, Cobitz AR, Waterhouse BR, Strachan MW. Improving metabolic control leads to better working memory in adults with type 2 diabetes. Diabetes Care 2006; 29: 345-351.
157. Abbatecola AM, Rizzo MR, Barbieri M, et al.Postprandial plasma glucose excursions and cognitive functioning in aged type 2 diabetics. Neurology 2006; 67: 235-240.
158. Mussell M, Hewer W, Kulzer B, Bergis K, Rist F. Effects of improved glycaemic control maintained for 3 months on cognitive function in patients with Type 2 diabetes. Diabet Med 2004; 21: 1253-1256.
159. Austin EJ, Deary IJ. Effects of repeated hypoglycemia on cognitive function: a psychometrically validated reanalysis of the Diabetes Control and Complications Trial data. Diabetes Care 1999; 22: 1273-1277.
160. Jacobson AM, Musen G, Ryan CM, et al. Long-term effect of diabetes and its treatment on cognitive function. N Engl J Med 2007; 356: 1842-1852.
161. Peters R, Beckett N, Forette F, et al. 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: 683-689.
162. Berk-Planken I, de Konig I, Stolk R, Jansen H, Hoogerbrugge N. Atorvastatin, diabetic dyslipidemia, and cognitive functioning. Diabetes Care 2002; 25: 1250-1251.
163. Colberg SR, Somma CT, Sechrist SR. Physical activity participation may offset some of the negative impact of diabetes on cognitive function. J Am Med Dir Assoc 2008; 9: 434-438.
164. Sandeep TC, Yau JL, MacLullich AM, et al. 11Beta-hydroxysteroid dehydrogenase inhibition improves cognitive function in healthy elderly men and type 2 diabetics. Proc Natl Acad Sci USA 2004; 101: 6734-6739.
165. Chui MH, Greenwood CE. Antioxidant vitamins reduce acute meal-induced memory deficits in adults with type 2 diabetes. Nutr Res 2008; 28: 423-429.
166. De Galan BE, Zoungas S, Chalmers J, et al. Cognitive function and risks of cardiovascular disease and hypoglycaemia in patients with type 2 diabetes: the action in diabetes and vascular disease: Preterax and diamicron modified release controlled evaluation (ADVANCE) trial. Diabetologia 2009; 52: 2328-2336.
167. Leibson CL, Rocca WA, Hanson VA, et al.Theriskofdementia among persons with diabetes mellitus: a population-based cohort study. Ann N Y Acad Sci 1997; 826: 422-427.