Structural and functional brain changes in middle-aged type 2 diabetic patients: A cross-sectional study

Journal of Alzheimer's Disease

Volumn 40, Issue 2, 2014, Pages 375-386

  García Casares, Natalia ^a,b   Berthier, Marcelo L ^a,b   Jorge, Ricardo E ^c   Gonzalez Alegre, Pedro ^c   Gutiérrez Cardo, Antonio ^b   Rioja Villodres, José ^a,b   Acion, Laura ^d   Ariza Corbo, María José ^a,b   Nabrozidis, Alejandro ^b   García Arnés, Juan A ^e   González Santos, Pedro ^a,b,f  

^a UNIVERSIDAD DE MÁLAGA   (Spain)

^b Centro de Investigaciones Médico Sanitarias C I M E S   (Spain)

^c UNIVERSITY OF IOWA   (United States)

^d UNIVERSITY OF IOWA   (United States)

^e HOSPITAL REGIONAL UNIVERSITARIO DE MÁLAGA   (Spain)

^f HOSPITAL UNIVERSITARIO VIRGEN DE LA VICTORIA   (Spain)

Author keywords

cognition; magnetic resonance imaging; neuroimaging; positron emission tomography; type 2 diabetes mellitus

Indexed keywords

ANTIHYPERTENSIVE AGENT; ANTILIPEMIC AGENT; FLUORODEOXYGLUCOSE F 18; GLUCOSE; HEMOGLOBIN A1C; INSULIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; ORAL ANTIDIABETIC AGENT; TRIACYLGLYCEROL; APOLIPOPROTEIN E;

ADULT; ADULT DISEASE; ANGULAR GYRUS; ANTERIOR CINGULATE; ANTIHYPERTENSIVE THERAPY; ARTICLE; BRAIN; BRAIN CORTEX; BRAIN FUNCTION; BRAIN MAPPING; BRAIN METABOLISM; BRAIN REGION; BRAIN SCINTISCANNING; BRAIN STRUCTURE; CARDIOVASCULAR RISK; CEREBRAL GLUCOSE METABOLISM; CHOLESTEROL BLOOD LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DENSITY; DIABETIC PATIENT; DISEASE DURATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; FUSIFORM GYRUS; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GLYCEMIC CONTROL; GRAY MATTER; HUMAN; HYPERTENSION; INFERIOR TEMPORAL GYRUS; INSULIN RESISTANCE; INSULIN TREATMENT; MALE; MIDDLE AGED; MIDDLE TEMPORAL GYRUS; NEUROIMAGING; NON INSULIN DEPENDENT DIABETES MELLITUS; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRECUNEUS; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIORITY JOURNAL; SMOKING; STRUCTURAL MAGNETIC RESONANCE IMAGING; STRUCTURAL NEUROIMAGING; SUPERIOR TEMPORAL GYRUS; TRIACYLGLYCEROL BLOOD LEVEL; VOXEL BASED MORPHOMETRY; AGED; BLOOD PRESSURE; CASE CONTROL STUDY; COMPLICATION; DIABETES MELLITUS, TYPE 2; GENETICS; IMAGE PROCESSING; PATHOLOGY; PATHOPHYSIOLOGY; SCINTISCANNING;

AGED; APOLIPOPROTEINS E; BLOOD PRESSURE; BRAIN; CASE-CONTROL STUDIES; CROSS-SECTIONAL STUDIES; DIABETES MELLITUS, TYPE 2; FEMALE; FLUORODEOXYGLUCOSE F18; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; POSITRON-EMISSION TOMOGRAPHY;

EID: 84901929243     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-131736     Document Type: Article

References (50)

1. 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 (Pubitemid 46588347)
2. Nooyens AC, Baan CA, Spijkerman AM, Verschuren WM (2010) T2DM and cognitive decline in middle-aged men and women: The Doetinchem Cohort Study. Diabetes Care 33, 1964-1969.
3. Reijmer YD, van den BergE, Ruis C, Kappelle LJ, Biessels GJ (2010) Cognitive dysfunction in patients with type 2 diabetes. Diabetes Metab Res Rev 26, 507-519.
4. Luchsinger JA (2012) Type 2 diabetes and cognitive impairment: Linking mechanisms. J Alzheimers Dis 30(Suppl 2), S185-S198.
5. S Roriz-Filho J, S'a-Roriz TM, Rosset I, Camozzato AL, Santos AC, Chaves ML, Moriguti JC, Roriz-Cruz M (2009) (Pre)diabetes, brain aging, and cognition. Biochim Biophys Acta 1792, 432-443.
6. Strachan MW, Reynolds RM, Marioni RE, Price JF (2011) Cognitive function, dementia and type 2 diabetes mellitus in the elderly. Nat Rev Endocrinol 7, 108-114.
7. Yaffe K, Lindquist K, Schwartz A, Vitartas C, Vittinghoff E, Satterfield S, Simonsick EM, Launer L, Rosano C, Cauley JA, Harris T (2011) Advanced glycation endproduct level, diabetes and accelerated cognitive aging. Alzheimers Dement 7(4 Suppl), S289.
8. de la MonteSM(2012) Brain insulin resistance and deficiency as therapeutic targets in Alzheimer's disease. Curr Alzheimer Res 9, 35-66.
9. Craft S (2009) The role of metabolic disorders in Alzheimer disease and vascular dementia: Two roads converged. Arch Neurol 66, 300-305.
10. de la Monte SM, TongM(2009) Mechanisms of nitrosaminemediated neurodegeneration: Potential relevance to sporadic Alzheimer's disease. J Alzheimers Dis 17, 817-825.
11. Ahtiluoto S, Polvikoski T, Peltonen M, Solomon A, Tuomilehto J, Winblad B, Sulkava R, Kivipelto M (2010) Diabetes, Alzheimer disease, and vascular dementia: A populationbased neuropathologic study. Neurology 75, 1195-1202.
12. Heitner J, Dickson D (1997) Diabetics do not have increased Alzheimer-type pathology compared with agematched control subjects. A retrospective postmortem immunocytochemical and histofluorescent study. Neurology 49, 1306-1311. (Pubitemid 27495634)
13. Nelson PT, Smith CD, Abner EA, Schmitt FA, Scheff SW, Davis GJ, Keller JN, Jicha GA, Davis D, Wang-Xia W, Hartman A, Katz DG, Markesbery WR (2009) Human cerebral neuropathology of Type 2 diabetes mellitus. Biochim Biophys Acta 1792, 454-469.
14. den Heijer T,Vermeer SE, van Dijk EJ,Koudstaal PJ, Hofman A, BretelerMM(2003) T2DM and atrophy of medial temporal lobe structures on brain MRI. Diabetologia 46, 1604-1610. (Pubitemid 38005322)
15. Brundel M, van den Heuvel M, de Bresser J, Kappelle LJ, Biessels GJ (2010) Cerebral cortical thickness in patients with T2DM. J Neurol Sci 299, 126-130.
16. 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 T2DM. Diabetes 55, 1106-1113. (Pubitemid 44100188)
17. de Bresser J, Tiehuis AM, van den Berg E, Reijmer YD, Jongen C, Kappelle LJ, Mali WP, Viergever MA, Biessels GJ (2010) Utrecht Diabetic Encephalopathy Study Group. Progression of cerebral atrophy and white matter hyperintensities in patients with type 2 diabetes. Diabetes Care 33, 1309- 1314.
18. Schmidt R, Launer LJ, Nilsson LG, Pajak A, Sans S, Berger K, Breteler MM, de Ridder M, Dufouil C, Fuhrer R, Giampaoli S, Hofman A CASCADE Consortium (2004) Magnetic resonance imaging of the brain in diabetes: The Cardiovascular Determinants of Dementia (CASCADE) Study. Diabetes 53, 687-692. (Pubitemid 38270638)
19. Brundel M, van den Berg E, Reijmer YD, de Bresser J, Kappelle LJ, Biessels GJ (2012) Utrecht Diabetic Encephalopathy Study group. Cerebral haemodynamics, cognition and brain volumes in patients with type 2 diabetes. J Diabetes Complications 26, 205-209.
20. Baker LD, Cross DJ, Minoshima S, Belongia D, Watson GS, Craft S (2011) Insulin resistance and alzheimer-like reductions in regional cerebral glucose metabolism for cognitively normal adults with prediabetes or early T2DM. Arch Neurol 68, 51-57.
21. Shtasel DL, Gur RE, Mozley PD, Richards J, Taleff MM, Heimberg C, Gallacher F, Gur RC (1991) Volunteers for biomedical research. Recruitment and screening of normal controls. Arch Gen Psychiatry 48, 1022-1025.
22. Genuth S, Alberti KG, Bennett P, Buse J, Defronzo R, Kahn R, Kitzmiller J, Knowler WC, Lebovitz H, Lernmark A, Nathan D, Palmer J, Rizza R, Saudek C, Shaw J, Steffes M, Stern M, Tuomilehto J, Zimmet P, Expert Committee on the Diagnosis and Classification of Diabetes Mellitus (2003) Follow-up report on the diagnosis of diabetes mellitus. Diabetes Care 26, 3160-3167. (Pubitemid 37339514)
23. Folstein MF, Folstein SE, McHugh PR (1975) "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12, 189-198.
24. Hindmarch I, Lehfeld H, De Jong P, Erzigkeit H (1971) The Bayer Activities of Daily Living Scale (B-ADL). Dement Geriatr Cogn Disord 9, 20-26.
25. Olfield RC (1971) The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9, 97-113.
26. ). National Institutes of Health. Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults. The evidence report. Obes Res 6(Suppl 2), 51S-209S.
27. Wilson PW, D'Agostino RB, Levy D (1998) Prediction of coronary heart disease using risk factor categories. Circulation 97, 1837-1847. (Pubitemid 28213628)
28. Tietz NW (1990) Clinical Guide to Laboratory Tests, 2nd edition. W. B. Saunders, Philadelphia, PA.
29. Koch W, Enrenhaft A, Griesser K, Pfeufer A, M?uller J, Sch?omig A, Kastrati A (2002) TaqMan systems for genotyping of disease-related polymorphisms present in the gene encoding apolipoprotein E. Clin Chem Lab Med 40, 1123- 1131. (Pubitemid 36032659)
30. Ashburner J, Friston KJ (2000) Voxel-based morphometry- the methods. Neuroimage 11, 805-821.
31. Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26, 839-851. (Pubitemid 40825026)
32. Waxman AD, Herholz K, Lewis DH, Herscovitch P, Minoshima S, Ichise M, Drzezga AE, Devous MD, Mountz JM (2009) Society of Nuclear Medicine Procedure Guideline for FDG PET brain imaging version 1.0. Available from http://interactive.snm.org/index.cfm?PageID=8490.
33. Rousset OG, Ma Y, Evans AC (1998) Correction for partial volume effects in PET: Principle and validation. J Nucl Med 39, 904-911. (Pubitemid 28216748)
34. Talairach J, Tournoux P (1988) Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System - an Approach to Cerebral Imaging, Thieme Medical Publishers, New York.
35. The Diabetes Control, Complications Research Group (1997) Hypoglycemia in the Diabetes Control and Complications Trial. Diabetes 46, 271-286.
36. Bruehl H, Wolf OT, Sweat V, Tirsi A, Richardson S, Convit A (2009) Modifiers of cognitive function and brain structure in middleaged and elderly individuals with T2DM mellitus. Brain 1280, 186-194.
37. Espeland MA, Bryan RN, Goveas JS, Robinson JG, Siddiqui MS, Liu S, Hogan PE, Casanova R, Coker LH, Yaffe K, Masaki K, Rossom R, Resnick SM, WHIMS-MRI Study Group (2013) 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 36, 90-97.
38. van Elderen SG, de Roos A, de Craen AJ, Westendorp RG, Blauw GJ, Jukema JW, Bollen EL, Middelkoop HA, van Buchem MA, van der Grond J (2010) Progression of brain atrophy and cognitive decline in diabetes mellitus: A 3-year follow-up. Neurology 75, 997-1002.
39. van Harten B, de Leeuw FE,Weinstein HC, Scheltens P, Biessels GJ (2006) Brain imaging in patients with diabetes: A systematic review. Diabetes Care 29, 2539-2548. (Pubitemid 44912267)
40. Kumar A, Haroon E, Darwin C (2008) Gray matter prefrontal changes inT2DMdetected using MRI. JMagn Reson Imaging 27, 14-19.
41. Chen Z, Li L, Sun J, Ma L (2012) Mapping the brain in type II diabetes: Voxel-based morphometry using DARTEL. Eur J Radiol 81, 1870-1876.
42. Musen G, Lyoo IK, Sparks CR, Weinger K, Hwang J, Ryan CM, Jimerson DC, Hennen J, Renshaw PF, Jacobson AM (2006) Effects of type 1 diabetes on gray matter density as measured by voxel-based morphometry. Diabetes 55, 326- 333. (Pubitemid 43343260)
43. Roberts RO, Geda YE, Knopman DS, Christianson TJ, Pankratz VS, Boeve BF, Vella A, Rocca WA, Petersen RC (2008) Association of duration and severity of diabetes mellitus with mild cognitive impairment. Arch Neurol 65, 1066- 1073.
44. Cukierman-Yaffe T, Gerstein HC,Williamson JD, Lazar RM, Lovato L, Miller ME, Coker LH, Murray A, Sullivan MD, Marcovina SM, Launer LJ (2009) Relationship between baseline glycemic control and cognitive function in individuals with T2DM and other cardiovascular risk factors: The action to control cardiovascular risk in diabetes-memory in diabetes (ACCORD-MIND) trial. Diabetes Care 32, 221-226.
45. Launer LJ, Miller ME, Williamson JD, Lazar RM, Gerstein HC, Murray AM, SullivanM, Horowitz KR, Ding J, Marcovina S, Lovato LC, Lovato J, Margolis KL, O'Connor P, Lipkin EW, Hirsch J, Coker L, Maldjian J, Sunshine JL, Truwit C, Davatzikos C, Bryan RN; ACCORD MIND investigators (2011) 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 10, 969-977.
46. Tomita N, Furukawa K, Okamura N, Tashiro M, Une K, Furumoto S, Iwata R, Yanai K, Kudo Y, Arai H (2013) Brain accumulation of amyloid - protein visualized by positron emission tomography and BF-227 in Alzheimer's disease patients with or without diabetes mellitus. Geriatr Gerontol Int 13, 215-221.
47. Talbot K, Wang HY, Kazi H, Han LY, Bakshi KP, Stucky A, Fuino RL, Kawaguchi KR, Samoyedny AJ, Wilson RS, Arvanitakis Z, Schneider JA, Wolf BA, Bennett DA, Trojanowski JQ, Arnold SE (2012) 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, 1316-1338.
48. Kuczynski B, Jagust W, Chui HC, Reed B (2009) An inverse association of cardiovascular risk and frontal lobe glucose metabolism. Neurology 72, 738-743.
49. 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. (Pubitemid 39577337)
50. Stewart R, Liolitsa D (1999) Type 2 diabetes mellitus, cognitive impairment and dementia. Diabet Med 16, 93-112.