Type 2 diabetes and cognitive impairment: Contributions from neuroimaging

Journal of Geriatric Psychiatry and Neurology

Volumn 27, Issue 1, 2014, Pages 47-55

  Ryan, John P ^a   Fine, David F ^b   Rosano, Caterina ^c  

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

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

cognitive impairment; neuroimaging; type 2 diabetes

Indexed keywords

BIOLOGICAL MARKER; INSULIN;

ALZHEIMER DISEASE; ARTICLE; BRAIN BLOOD FLOW; COGNITION; COGNITIVE DEFECT; DIFFUSION TENSOR IMAGING; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; NEUROIMAGING; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOPHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RISK FACTOR; WHITE MATTER;

COGNITIVE IMPAIRMENT; NEUROIMAGING; TYPE 2 DIABETES;

AGED; AGING; ALZHEIMER DISEASE; BRAIN; COGNITION DISORDERS; DIABETES MELLITUS, TYPE 2; DIFFUSION TENSOR IMAGING; HUMANS; NEURAL PATHWAYS; NEUROIMAGING; RISK FACTORS;

EID: 84893547501     PISSN: 08919887     EISSN: 15525708     Source Type: Journal    
DOI: 10.1177/0891988713516543     Document Type: Article

References (67)

1. National Diabetes Fact Sheet: National Estimates and General Information on Diabetes and Prediabetes in the United States, 2011. Atlanta, GA: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention ; 2011 :
2. Hebert LE, Scherr PA, Bienias JL, Bennett DA, Evans DA. Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch Neurol. 2003 ; 60 (8). 1119-1122
3. Stumvoll M, Goldstein BJ, van Haeften TW. Type 2 diabetes: pathogenesis and treatment. Lancet. 2008 ; 371 (9631). 2153-2156
4. Dartigues JF. Alzheimer's disease: a global challenge for the 21st century. Lancet Neurol. 2009 ; 8 (12). 1082-1083
5. Reitz C, Brayne C, Mayeux R. Epidemiology of Alzheimer disease. Nat Rev Neurol. 2011 ; 7 (3). 137-152
6. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl). 1991 ; 82 (4). 239-259
7. Thompson PM, Hayashi KM, Dutton RA, et al. Tracking Alzheimer's disease. Ann N Y Acad Sci. 2007 ; 1097 (1). 183-214
8. Cole AR, Astell A, Green C, Sutherland C. Molecular connexions between dementia and diabetes. Neurosci Biobehav Rev. 2007 ; 31 (7). 1046-1063
9. Sims-Robinson C, Kim B, Rosko A, Feldman EL. How does diabetes accelerate Alzheimer disease pathology?. Nat Rev Neurol. 2010 ; 6 (10). 551-559
10. Zhang Y, Zhou B, Deng B, et al. Amyloid-β induces hepatic insulin resistance in vivo via JAK2. Diabetes. 2013 ; 62 (4). 1159-1166
11. 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
12. 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
13. Malek-Ahmadi M, Beach T, Obradov A, et al. Increased Alzheimer's disease neuropathology is associated with type 2 diabetes and ApoE â̂Š .4 carrier status. Curr Alzheimer Res. 2013 ; 10 (6). 654-659
14. Exalto LG, Whitmer RA, Kappele LJ, Biessels GJ. An update on type 2 diabetes, vascular dementia and Alzheimer's disease. Exp Gerontol. 2012 ; 47 (11). 858-864
15. Cukierman T, Gerstein HC, Williamson JD. Cognitive decline and dementia in diabetes - systematic overview of prospective observational studies. Diabetologia. 2005 ; 48 (12). 2460-2469
16. Fontbonne A, Berr C, Ducimetière P, Alpérovitch 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 (2). 366-370
17. 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 (12). 1327-1333
18. Van den Berg E, Reijmer YD, de Bresser J, et al. A 4 year follow-up study of cognitive functioning in patients with type 2 diabetes mellitus. Diabetologia. 2010 ; 53 (1). 58-65
19. Biessels GJ, Deary IJ, Ryan CM. Cognition and diabetes: a lifespan perspective. Lancet Neurol. 2008 ; 7 (2). 184-190
20. Van den Berg E, Kloppenborg RP, Kessels RPC, 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 (5). 470-481
21. Van Harten B, Oosterman J, Muslimovic D, van Loon B-JP, Scheltens P, Weinstein HC. Cognitive impairment and MRI correlates in the elderly patients with type 2 diabetes mellitus. Age Ageing. 2007 ; 36 (2). 164-170
22. 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
23. Schmidt R, Launer LJ, Nilsson L-G, et al. Magnetic resonance imaging of the brain in diabetes: the Cardiovascular Determinants of Dementia (CASCADE) Study. Diabetes. 2004 ; 53 (3). 687-692
24. Kumar R, Anstey KJ, Cherbuin N, Wen W, Sachdev PS. Association of type 2 diabetes with depression, brain atrophy, and reduced fine motor speed in a 60- to 64-year-old community sample. Am J Geriatr Psychiatry Off J Am Assoc Geriatr Psychiatry. 2008 ; 16 (12). 989-998
25. Biessels GJ, Koffeman A, Scheltens P. Diabetes and cognitive impairment. Clinical diagnosis and brain imaging in patients attending a memory clinic. J Neurol. 2006 ; 253 (4). 477-482
26. 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
27. Strachan MW, Reynolds RM, Marioni RE, Price JF. Cognitive function, dementia and type 2 diabetes mellitus in the elderly. Nat Rev Endocrinol. 2011 ; 7 (2). 108-114
28. Bruehl H, Wolf OT, Sweat V, Tirsi A, Richardson S, Convit A. Modifiers of cognitive function and brain structure in middle-aged and elderly individuals with type 2 diabetes mellitus. Brain Res. 2009 ; 1280: 186-194
29. 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
30. 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 (4). 1106-1113
31. Moran C, Phan TG, Chen J, et al. Brain atrophy in type 2 diabetes: Regional distribution and influence on cognition. Diabetes Care. 2013 ; 36 (12). 4036-4042
32. Reijmer YD, van den Berg E, de Bresser J, et al. Accelerated cognitive decline in patients with type 2 diabetes: MRI correlates and risk factors. Diabetes Metab Res Rev. 2011 ; 27 (2). 195-202
33. Espeland MA, Bryan RN, Goveas JS, et al. Influence of type 2 diabetes on brain volumes and changes in brain volumes: results from the Women's Health Initiative Magnetic Resonance Imaging studies. Diabetes Care. 2013 ; 36 (1). 90-97
34. Yau PL, Javier D, Tsui W, et al. Emotional and neutral declarative memory impairments and associated white matter microstructural abnormalities in adults with type 2 diabetes. Psychiatry Res. 2009 ; 174 (3). 223-230
35. Hsu JL, Chen YL, Leu JG, et al. Microstructural white matter abnormalities in type 2 diabetes mellitus: a diffusion tensor imaging study. Neuroimage. 2012 ; 59 (2). 1098-1105
36. Reijmer YD, Brundel M, de Bresser J, et al. Microstructural white matter abnormalities and cognitive functioning in type 2 diabetes: a diffusion tensor imaging study. Diabetes Care. 2013 ; 36 (1). 137-144
37. Bullmore ET, Bassett DS. Brain graphs: graphical models of the human brain connectome. Annu Rev Clin Psychol. 2011 ; 7: 113-140
38. Nagamachi S, Nishikawa T, Ono S, et al. Regional cerebral blood flow in diabetic patients: evaluation by N-isopropyl-123I-IMP with SPECT. Nucl Med Commun. 1994 ; 15 (6). 455-460
39. Sabri O, Hellwig D, Schreckenberger M, et al. Influence of diabetes mellitus on regional cerebral glucose metabolism and regional cerebral blood flow. Nucl Med Commun. 2000 ; 21 (1). 19-29
40. Tiehuis AM, Vincken KL, van den Berg E, et al. Cerebral perfusion in relation to cognitive function and type 2 diabetes. Diabetologia. 2008 ; 51 (7). 1321-1326
41. Brundel M, van den Berg E, Reijmer YD, de Bresser J, Kappelle LJ, Biessels GJ. Cerebral haemodynamics, cognition and brain volumes in patients with type 2 diabetes. J Diabetes Complications. 2012 ; 26 (3). 205-209
42. 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 (1). 58-65
43. Beason-Held LL, Thambisetty M, Deib G, et al. Baseline cardiovascular risk predicts subsequent changes in resting brain function. Stroke J Cereb Circ. 2012 ; 43 (6). 1542-1547
44. Thambisetty M, Beason-Held LL, An Y, et al. Impaired glucose tolerance in midlife and longitudinal changes in brain function during aging. Neurobiol Aging. 2013 ; 34 (10). 2271-2276
45. 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
46. Greicius M, Krasnow B, Reiss A, Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci U S A. 2003 ; 100 (1). 253-258
47. Kelly C, Biswal BB, Craddock RC, Castellanos FX, Milham MP. Characterizing variation in the functional connectome: promise and pitfalls. Trends Cogn Sci. 2012 ; 16 (3). 181-188
48. Zhou H, Lu W, Shi Y, et al. Impairments in cognition and resting-state connectivity of the hippocampus in elderly subjects with type 2 diabetes. Neurosci Lett. 2010 ; 473 (1). 5-10
49. Musen G, Jacobson AM, Bolo NR, et al. Resting-state brain functional connectivity is altered in type 2 diabetes. Diabetes. 2012 ; 61 (9). 2375-2379
50. Xia W, Wang S, Sun Z, et al. Altered baseline brain activity in type 2 diabetes: a resting-state fMRI study. Psychoneuroendocrinology. 2013 ; 38 (11). 2493-2501
51. Biessels GJ, De Leeuw FE, Lindeboom J, Barkhof F, Scheltens P. Increased cortical atrophy in patients with Alzheimer's disease and type 2 diabetes mellitus. J Neurol Neurosurg Psychiatry. 2006 ; 77 (3). 304-307
52. Thambisetty M, Metter EJ, 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
53. Craft S, Foster TC, Landfield PW, Maier SF, Resnick SM, Yaffe K., Session. Mechanisms of age-related cognitive change and targets for intervention: inflammatory, oxidative, and metabolic processes. J Gerontol A Biol Sci Med Sci. 2012 ; 67 (7). 754-759
54. Nelson PT, Smith CD, Abner EA, et al. Human cerebral neuropathology of Type 2 diabetes mellitus. Biochim Biophys Acta. 2009 ; 1792 (5). 454-469
55. Craft S, Peskind E, Schwartz MW, Schellenberg GD, Raskind M, Porte D. Cerebrospinal fluid and plasma insulin levels in Alzheimer's disease: relationship to severity of dementia and apolipoprotein E genotype. Neurology. 1998 ; 50 (1). 164-168
56. McNay EC, Ong CT, McCrimmon RJ, Cresswell J, Bogan JS, Sherwin RS. Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiol Learn Mem. 2010 ; 93 (4). 546-553
57. Reger MA, Watson GS, Green PS, et al. Intranasal insulin improves cognition and modulates beta-amyloid in early AD. Neurology. 2008 ; 70 (6). 440-448
58. Craft S, Baker LD, Montine TJ, et al. Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Arch Neurol. 2012 ; 69 (1). 29-38
59. Luchsinger JA, Small S, Biessels GJ. Should we target insulin resistance to prevent dementia due to Alzheimer disease?. Arch Neurol. 2011 ; 68 (1). 17-18
60. Watson GS, Cholerton BA, Reger MA, et al. Preserved cognition in patients with early Alzheimer disease and amnestic mild cognitive impairment during treatment with rosiglitazone: a preliminary study. Am J Geriatr Psychiatry. 2005 ; 13 (11). 950-958
61. Gold M, Alderton C, Zvartau-Hind M, et al. Rosiglitazone monotherapy in mild-to-moderate Alzheimer's disease: results from a randomized, double-blind, placebo-controlled phase III study. Dement Geriatr Cogn Disord. 2010 ; 30 (2). 131-146
62. Hsu CC, Wahlqvist ML, Lee MS, Tsai HN. Incidence of dementia is increased in type 2 diabetes and reduced by the use of sulfonylureas and metformin. J Alzheimers Dis. 2011 ; 24 (3). 485-493
63. Imfeld P, Bodmer M, Jick SS, Meier CR. Metformin, other antidiabetic drugs, and risk of Alzheimer's disease: a population-based case-control study. J Am Geriatr Soc. 2012 ; 60 (5). 916-921
64. Moore EM, Mander AG, Ames D, et al. Increased risk of cognitive impairment in patients with diabetes is associated with metformin. Diabetes Care. 2013 ; 36 (10). 2981-2987
65. Hunter K, Hölscher C. Drugs developed to treat diabetes, liraglutide and lixisenatide, cross the blood brain barrier and enhance neurogenesis. BMC Neurosci. 2012 ; 13: 33
66. During MJ, Cao L, Zuzga DS, et al. Glucagon-like peptide-1 receptor is involved in learning and neuroprotection. Nat Med. 2003 ; 9 (9). 1173-1179
67. McClean PL, Parthsarathy V, Faivre E, Hölscher C. The diabetes drug liraglutide prevents degenerative processes in a mouse model of Alzheimer's disease. J Neurosci Off J Soc Neurosci. 2011 ; 31 (17). 6587-6594