Skip to main content

Advertisement

Log in

Cardiovascular risk in cognitively preserved elderlies is associated with glucose hypometabolism in the posterior cingulate cortex and precuneus regardless of brain atrophy and apolipoprotein gene variations

  • Published:
AGE Aims and scope Submit manuscript

Abstract

Cardiovascular risk factors (CVRF) possibly contribute to the emergence of Alzheimer's disease (AD). Fluorodeoxyglucose-positron emission tomography (FDG-PET) has been widely used to demonstrate specific patterns of reduced cerebral metabolic rates of glucose (CMRgl) in subjects with AD and in non-demented carriers of the apolipoprotein ε4 (APOE ε4) allele, the major genetic risk factor for AD. However, functional neuroimaging studies investigating the impact of CVRF on cerebral metabolism have been scarce to date. The present FDG-PET study investigated 59 cognitively preserved elderlies divided into three groups according to their cardiovascular risk based on the Framingham 10-year risk Coronary Heart Disease Risk Profile (low-, medium-, and high-risk) to examine whether different levels of CVRF would be associated with reduced CMRgl, involving the same brain regions affected in early stages of AD. Functional imaging data were corrected for partial volume effects to avoid confounding effects due to regional brain atrophy, and all analyses included the presence of the APOE ε4 allele as a confounding covariate. Significant cerebral metabolism reductions were detected in the high-risk group when compared to the low-risk group in the left precuneus and posterior cingulate gyrus. This suggests that findings of brain hypometabolism similar to those seen in subjects with AD can be detected in association with the severity of cardiovascular risk in cognitively preserved individuals. Thus, a greater knowledge about how such factors influence brain functioning in healthy subjects over time may provide important insigths for the future development of strategies aimed at delaying or preventing the vascular-related triggering of pathologic brain changes in the AD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Acosta-Cabronero J, Williams GB, Pereira JM, Pengas G, Nestor PJ (2008) The impact of skull-stripping and radio-frequency bias correction on grey-matter segmentation for voxel-based morphometry. NeuroImage 39:1654–1665

    Article  PubMed  Google Scholar 

  • Alves TC, Rays J, Fraguas R Jr, Wajngarten M, Meneghetti JC, Prando S et al (2005) Localized cerebral blood flow reductions in patients with heart failure: a study using 99mTc-HMPAO SPECT. J Neuroimaging 15:150–156

    Article  PubMed  Google Scholar 

  • Andreason PJ, Zametkin AJ, Guo AC, Baldwin P, Cohen RM (1994) Gender-related differences in regional cerebral glucose metabolism in normal volunteers. Psychiatry Res 51:175–183

    Article  CAS  PubMed  Google Scholar 

  • 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 type 2 diabetes. Arch Neurol 68:51–57

    Article  PubMed Central  PubMed  Google Scholar 

  • Bangen KJ, Restom K, Liu TT, Jak AJ, Wierenga CE, Salmon DP et al (2009) Differential age effects on cerebral blood flow and BOLD response to encoding: associations with cognition and stroke risk. Neurobiol Aging 30:1276–1287

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bartenstein P, Asenbaum S, Catafau A, Halldin C, Pilowski L, Pupi A et al (2002) European Association of Nuclear Medicine procedure guidelines for brain imaging using [(18)F]FDG. Eur J Nucl Med Mol Imaging 29:BP43–BP48

    CAS  PubMed  Google Scholar 

  • Baxter LR Jr, Mazziotta JC, Phelps ME, Selin CE, Guze BH, Fairbanks L (1987) Cerebral glucose metabolic rates in normal human females versus normal males. Psychiatry Res 21:237–245

    Article  PubMed  Google Scholar 

  • Bell RD, Deane R, Chow N, Long X, Sagare A, Singh I et al (2009) SRF and myocardin regulate LRP-mediated amyloid-beta clearance in brain vascular cells. Nat Cell Biol 11:143–153

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brett M, Johnsrude IS, Owen AM (2002) The problem of functional localization in the human brain [Review]. Nat Rev Neurosci 3:243–249

    Article  CAS  PubMed  Google Scholar 

  • Chételat G, Desgranges B, de la Sayette V, Viader F, Berkouk K, Landeau B et al (2003) Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain 126:1955–1967

    Article  PubMed  Google Scholar 

  • Choi BR, Lee SR, Han JS, Woo SK, Kim KM, Choi DH et al (2011) Synergistic memory impairment through the interaction of chronic cerebral hypoperfusion and amlyloid toxicity in a rat model. Stroke 42:2595–2604

    Article  PubMed  Google Scholar 

  • Copeland JR, Dewey ME, Griffiths-Jones HM (1986) A computerized psychiatric diagnostic system and case nomenclature for elderly subjects: GMS and AGECAT. Psychol Med 16:89–99

    Article  CAS  PubMed  Google Scholar 

  • Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW et al (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261:921–923

    Article  CAS  PubMed  Google Scholar 

  • Craft S (2009) The role of metabolic disorders in Alzheimer disease and vascular dementia: two roads converged [Review]. Arch Neurol 66:300–305

    Article  PubMed Central  PubMed  Google Scholar 

  • Curiati PK, Tamashiro-Duran JH, Duran FL, Buchpiguel CA, Squarzoni P, Romano DC et al (2011) Age-related metabolic profiles in cognitively healthy elders: results from a voxel-based [18F]fluorodeoxyglucose-positron-emission tomography study with partial volume effects correction. AJNR Am J Neuroradiol 32:560–565

    Article  CAS  PubMed  Google Scholar 

  • de la Torre JC (1999) Critical threshold cerebral hypoperfusion causes Alzheimer's disease? [Review]. Acta Neuropathol 98:1–8

    Article  PubMed  Google Scholar 

  • de la Torre JC (2009) Cerebrovascular and cardiovascular pathology in Alzheimer's disease [Review]. Int Rev Neurobiol 84:35–48

    Article  CAS  PubMed  Google Scholar 

  • de la Torre JC, Mussivand T (1993) Can disturbed brain microcirculation cause Alzheimer's disease? [Review]. Neurol Res 15:146–153

    PubMed  Google Scholar 

  • de la Torre JC, Pappas BA, Prevot V, Emmerling MR, Mantione K, Fortin T et al (2003) Hippocampal nitric oxide upregulation precedes memory loss and A beta 1–40 accumulation after chronic brain hypoperfusion in rats. Neurol Res 25:635–641

    Article  PubMed  Google Scholar 

  • de Toledo Ferraz Alves TC, Scazufca M, Squarzoni P, de Souza Duran FL, Tamashiro-Duran JH, Vallada HP et al (2011) Subtle gray matter changes in temporo-parietal cortex associated with cardiovascular risk factors. J Alzheimers Dis 27:575–589

    PubMed  Google Scholar 

  • Drzezga A, Grimmer T, Riemenschneider M, Lautenschlager N, Siebner H, Alexopoulus P et al (2005) Prediction of individual clinical outcome in MCI by means of genetic assessment and (18)F-FDG PET. J Nucl Med 46:1625–1632

    CAS  PubMed  Google Scholar 

  • Elias MF, Elias PK, D'Agostino RB, Silbershatz H, Wolf PA (1997) Role of age, education, and gender on cognitive performance in the Framingham Heart Study: community-based norms. Exp Aging Res 23:201–235

    Article  CAS  PubMed  Google Scholar 

  • Eriksson SH, Thom M, Symms MR, Focke NK, Martinian L, Sisodiya SM et al (2009) Cortical neuronal loss and hippocampal sclerosis are not detected by voxel-based morphometry in individual epilepsy surgery patients. Hum Brain Mapp 30:3351–3360

    Article  PubMed Central  PubMed  Google Scholar 

  • Erkinjuntti T, Gauthier S (2009) The concept of vascular cognitive impairment [Review]. Front Neurol Neurosci 24:79–85

    Article  PubMed  Google Scholar 

  • Faul F, Erdfelder E, Lang AG, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39:175–191

    Article  PubMed  Google Scholar 

  • Fitzpatrick AL, Kuller LH, Lopez OL, Diehr P, O'Meara ES, Longstreth WT Jr et al (2009) Midlife and late-life obesity and the risk of dementia: cardiovascular health study. Arch Neurol 66:336–342

    Article  PubMed Central  PubMed  Google Scholar 

  • Friston KJ, Holmes A, Poline JB, Price CJ, Frith CD (1996) Detecting activations in PET and fMRI: levels of inference and power. NeuroImage 4:223–235

    Article  CAS  PubMed  Google Scholar 

  • Fujimoto T, Matsumoto T, Fujita S, Takeuchi K, Nakamura K, Mitsuyama Y et al (2008) Changes in glucose metabolism due to aging and gender-related differences in the healthy human brain. Psychiatry Res 164:58–72

    Article  CAS  PubMed  Google Scholar 

  • Gimbrone MA Jr (1999) Endothelial dysfunction, hemodynamic forces, and atherosclerosis [Review]. Thromb Haemost 82:722–726

    CAS  PubMed  Google Scholar 

  • Gimbrone MA (2010) The Gordon Wilson lecture. Understanding vascular endothelium: a pilgrim's progress. Endothelial dysfunction, biomechanical forces and the pathobiology of atherosclerosis. Trans Am Clin Climatol Assoc 121:115–127

    PubMed Central  PubMed  Google Scholar 

  • Gorelick PB (2004) Risk factors for vascular dementia and Alzheimer disease [Review]. Stroke 35:2620–2622

    Article  PubMed  Google Scholar 

  • Grammas P (2000) A damaged microcirculation contributes to neuronal cell death in Alzheimer's disease [Review]. Neurobiol Aging 21:199–205

    Article  CAS  PubMed  Google Scholar 

  • Grammas P (2011) Neurovascular dysfunction, inflammation and endothelial activation: implications for the pathogenesis of Alzheimer's disease. [Review]. J Neuroinflammation 8:26

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grammas P, Martinez J, Miller B (2011) Cerebral microvascular endothelium and the pathogenesis of neurodegenerative diseases. [Review]. Expert Rev Mol Med 13:e19

    Article  CAS  PubMed  Google Scholar 

  • Irie F, Fitzpatrick AL, Lopez OL, Kuller LH, Peila R, Newman AB et al (2008) Enhanced risk for Alzheimer disease in persons with type 2 diabetes and APOE epsilon4: the Cardiovascular Health Study Cognition Study. Arch Neurol 65:89–93

    Article  PubMed  Google Scholar 

  • Ishii H, Ishikawa H, Meguro K, Tashiro M, Yamaguchi S (2009) Decreased cortical glucose metabolism in converters from CDR 0.5 to Alzheimer's disease in a community: the Osaki-Tajiri Project. Int Psychogeriatr 21:148–156

    Article  PubMed  Google Scholar 

  • Jagust W (2006) Positron emission tomography and magnetic resonance imaging in the diagnosis and prediction of dementia [Review]. Alzheimers Dement 2:36–42

    Article  PubMed  Google Scholar 

  • Jeerakathil T, Wolf PA, Beiser A, Massaro J, Seshadri S, D'Agostino RB et al (2004) Stroke risk profile predicts white matter hyperintensity volume: the Framingham Study. Stroke 35:1857–1861

    Article  PubMed  Google Scholar 

  • Kawachi T, Ishii K, Sakamoto S, Sasaki M, Mori T, Yamashita F et al (2006) Comparison of the diagnostic performance of FDG-PET and VBM-MRI in very mild Alzheimer's disease. Eur J Nucl Med Mol Imaging 33:801–809

    Article  PubMed  Google Scholar 

  • Kitagawa K (2010) Cerebral blood flow measurement by PET in hypertensive subjects as a marker of cognitive decline [Review]. J Alzheimers Dis 20:855–859

    PubMed  Google Scholar 

  • Kivipelto M, Rovio S, Ngandu T, Kareholt I, Eskelinen M, Winblad B et al (2008) Apolipoprotein E epsilon4 magnifies lifestyle risks for dementia: a population-based study. J Cell Mol Med 12:2762–2771

    Article  CAS  PubMed  Google Scholar 

  • Knopman D, Boland LL, Mosley T, Howard G, Liao D, Szklo M et al (2001) Cardiovascular risk factors and cognitive decline in middle-aged adults. Neurology 56:42–48

    Article  CAS  PubMed  Google Scholar 

  • Kuczynski B, Jagust W, Chui HC, Reed B (2009) An inverse association of cardiovascular risk and frontal lobe glucose metabolism. Neurology 72:738–743

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kumar-Singh S (2008) Cerebral amyloid angiopathy: pathogenetic mechanisms and link to dense amyloid plaques [Review]. Genes Brain Behav 7:67–82

    Article  CAS  PubMed  Google Scholar 

  • Langbaum JB, Chen K, Caselli RJ, Lee W, Reschke C, Bandy D et al (2010) Hypometabolism in Alzheimer-affected brain regions in cognitively healthy Latino individuals carrying the apolipoprotein E epsilon4 allele. Arch Neurol 67:462–468

    Article  PubMed Central  PubMed  Google Scholar 

  • Langbaum JB, Chen K, Launer LJ, Fleisher AS, Lee W, Liu X et al (2012) Blood pressure is associated with higher brain amyloid burden and lower glucose metabolism in healthy late middle-age persons. Neurobiol Aging 33:827.e11–9

    Article  CAS  Google Scholar 

  • Launer LJ, Ross GW, Petrovitch H, Masaki K, Foley D, White LR et al (2000) Midlife blood pressure and dementia: the Honolulu-Asia aging study. Neurobiol Aging 21:49–55

    Article  CAS  PubMed  Google Scholar 

  • Li J, Wang YJ, Zhang M, Xu ZQ, Gao CY, Fang CQ et al (2011) Vascular risk factors promote conversion from mild cognitive impairment to Alzheimer disease. Neurology 76:1485–1491

    Article  CAS  PubMed  Google Scholar 

  • Libby P (2009) Molecular and cellular mechanisms of the thrombotic complications of atherosclerosis [Review]. J Lipid Res 50:S352–S357

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Massaro JM, D'Agostino RB Sr, Sullivan LM, Beiser A, DeCarli C, Au R et al (2004) Managing and analysing data from a large-scale study on Framingham Offspring relating brain structure to cognitive function. Stat Med 23:351–367

    Article  PubMed  Google Scholar 

  • Meigs JB, Singer DE, Sullivan LM, Dukes KA, D'Agostino RB, Nathan DM et al (1997) Metabolic control and prevalent cardiovascular disease in non-insulin-dependent diabetes mellitus (NIDDM): the NIDDM Patient Outcome Research Team. Am J Med 102:38–47

    Article  CAS  PubMed  Google Scholar 

  • Meltzer CC, Cantwell MN, Greer PJ, Ben-Eliezer D, Smith G, Frank G et al (2000) Does cerebral blood flow decline in healthy aging? A PET study with partial-volume correction. J Nucl Med 41:1842–1848

    CAS  PubMed  Google Scholar 

  • Menon U, Kelley RE (2009) Subcortical ischemic cerebrovascular dementia [Review]. Int Rev Neurobiol 84:21–33

    Article  PubMed  Google Scholar 

  • Mesulam MM (1999) Neuroplasticity failure in Alzheimer's disease: bridging the gap between plaques and tangles [Review]. Neuron 24:521–529

    Article  CAS  PubMed  Google Scholar 

  • Meyer JS, Rauch GM, Rauch RA, Haque A, Crawford K (2000) Cardiovascular and other risk factors for Alzheimer's disease and vascular dementia. Ann N Y Acad Sci 903:411–423

    Article  CAS  PubMed  Google Scholar 

  • Minoshima S, Giordani B, Berent S, Frey KA, Foster NL, Kuhl DE (1997) Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann Neurol 42:85–94

    Article  CAS  PubMed  Google Scholar 

  • Mosconi L (2005) Brain glucose metabolism in the early and specific diagnosis of Alzheimer's disease. FDG-PET studies in MCI and AD [Review]. Eur J Nucl Med Mol Imaging 32:486–510

    Article  CAS  PubMed  Google Scholar 

  • Mosconi L, De Santi S, Rusinek H, Convit A, de Leon MJ (2004) Magnetic resonance and PET studies in the early diagnosis of Alzheimer's disease [Review]. Expert Rev Neurother 4:831–849

    Article  PubMed  Google Scholar 

  • Mosconi L, Tsui WH, Herholz K, Pupi A, Drzezga A, Lucignani G et al (2008a) Multicenter standardized 18F-FDG PET diagnosis of mild cognitive impairment, Alzheimer's disease, and other dementias. J Nucl Med 49:390–398

    Article  PubMed Central  PubMed  Google Scholar 

  • Mosconi L, De Santi S, Brys M, Tsui WH, Pirraglia E, Glodzik-Sobanska L et al (2008b) Hypometabolism and altered cerebrospinal fluid markers in normal apolipoprotein E E4 carriers with subjective memory complaints. Biol Psychiatry 63:609–618

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Obisesan TO, Obisesan OA, Martins S, Alamgir L, Bond V, Maxwell C et al (2008) High blood pressure, hypertension, and high pulse pressure are associated with poorer cognitive function in persons aged 60 and older: the Third National Health and Nutrition Examination Survey. J Am Geriatr Soc 56:501–509

    Article  PubMed Central  PubMed  Google Scholar 

  • Pereira JM, Xiong L, Acosta-Cabronero J, Pengas G, Williams GB, Nestor PJ (2010) Registration accuracy for VBM studies varies according to region and degenerative disease grouping. NeuroImage 49:2205–2215

    Article  CAS  PubMed  Google Scholar 

  • Petrie EC, Cross DJ, Galasko D, Schellenberg GD, Raskind MA, Peskind ER et al (2009) Preclinical evidence of Alzheimer changes: convergent cerebrospinal fluid biomarker and fluorodeoxyglucose positron emission tomography findings. Arch Neurol 66:632–637

    Article  PubMed Central  PubMed  Google Scholar 

  • Prince M, Ferri CP, Acosta D, Albanese E, Arizaga R, Dewey M et al (2007) The protocols for the 10/66 dementia research group population-based research programme. BMC Publ Health 7:165

    Article  Google Scholar 

  • Qiu C, Kivipelto M, von Strauss E (2009) Epidemiology of Alzheimer's disease: occurrence, determinants, and strategies toward intervention [Review]. Dialogues Clin Neurosci 11:111–128

    PubMed Central  PubMed  Google Scholar 

  • Quarantelli M, Berkouk K, Prinster A, Landeau B, Svarer C, Balkay L et al (2004) Integrated software for the analysis of brain PET/SPECT studies with partial-volume-effect correction. J Nucl Med 45:192–201

    PubMed  Google Scholar 

  • Razay G, Vreugdenhil A, Wilcock G (2007) The metabolic syndrome and Alzheimer disease. Arch Neurol 64:93–96

    Article  PubMed  Google Scholar 

  • Reiman EM, Chen K, Alexander GE, Caselli RJ, Bandy D, Osborne D et al (2004) Functional brain abnormalities in young adults at genetic risk for late-onset Alzheimer's dementia. Proc Natl Acad Sci U S A 101:284–289

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reiman EM, Chen K, Langbaum JB, Lee W, Reschke C, Bandy D et al (2010) Higher serum total cholesterol levels in late middle age are associated with glucose hypometabolism in brain regions affected by Alzheimer's disease and normal aging. NeuroImage 49:169–176

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rosendorff C, Beeri MS, Silverman JM (2007) Cardiovascular risk factors for Alzheimer's disease [Review]. Am J Geriatr Cardiol 16:143–149

    Article  PubMed  Google Scholar 

  • Salmina AB, Inzhutova AI, Malinovskaya NA, Petrova MM (2010) Endothelial dysfunction and repair in Alzheimer-type neurodegeneration: neuronal and glial control [Review]. J Alzheimers Dis 22:17–36

    PubMed  Google Scholar 

  • Scazufca M, Seabra CA (2008) Sao Paulo portraits: ageing in a large metropolis. Int J Epidemiol 37:721–723

    Article  PubMed  Google Scholar 

  • Scazufca M, Menezes PR, Vallada HP, Crepaldi AL, Pastor-Valero M, Coutinho LM et al (2008) High prevalence of dementia among older adults from poor socioeconomic backgrounds in Sao Paulo, Brazil. Int Psychogeriatr 20:394–405

    Article  PubMed  Google Scholar 

  • Seshadri S (2006) Methodology for measuring cerebrovascular disease burden [Review]. Int Rev Psychiatry 18:409–422

    Article  PubMed  Google Scholar 

  • Seshadri S, Wolf PA, Beiser A, Elias MF, Au R, Kase CS et al (2004) Stroke risk profile, brain volume, and cognitive function: the Framingham Offspring Study. Neurology 63:1591–1599

    Article  CAS  PubMed  Google Scholar 

  • Smith SM, De Stefano N, Jenkinson M, Matthews PM (2001) Normalized accurate measurement of longitudinal brain change. J Comput Assist Tomogr 25:466–475

    Article  CAS  PubMed  Google Scholar 

  • Smith SM, Zhang Y, Jenkinson M, Chen J, Matthews PM, Federico A, et al (2002) Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage 17:479–489

    Google Scholar 

  • Stuerenburg HJ, Ganzer S, Arlt S, Muller-Thomsen T (2005) The influence of smoking on plasma folate and lipoproteins in Alzheimer disease, mild cognitive impairment and depression. Neuro Endocrinol Lett 26:261–263

    CAS  PubMed  Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme Medical, New York

    Google Scholar 

  • Teipel SJ, Meindl T, Wagner M, Kohl T, Burger K, Reiser MF et al (2009) White matter microstructure in relation to education in aging and Alzheimer's disease. J Alzheimers Dis 17:571–583

    PubMed  Google Scholar 

  • Vander Borght T, Laloux P, Maes A, Salmon E, Goethals I, Goldman S (2001) Guidelines for brain radionuclide imaging. Perfusion single photon computed tomography (SPECT) using Tc-99m radiopharmaceuticals and brain metabolism positron emission tomography (PET) using F-18 fluorodeoxyglucose. The Belgian Society for Nuclear Medicine. Acta Neurol Belg 101:196–209

    CAS  PubMed  Google Scholar 

  • Viswanathan A, Rocca WA, Tzourio C (2009) Vascular risk factors and dementia: how to move forward? [Review]. Neurology 72:368–374

    Article  PubMed Central  PubMed  Google Scholar 

  • Volkow ND, Wang GJ, Telang F, Fowler JS, Goldstein RZ, Alia-Klein N et al (2009) Inverse association between BMI and prefrontal metabolic activity in healthy adults. Obesity 17:60–65

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang X, Xing A, Xu C, Cai Q, Liu H, Li L (2010) Cerebrovascular hypoperfusion induces spatial memory impairment, synaptic changes, and amyloid-beta oligomerization in rats. J Alzheimers Dis 21:813–822

    CAS  PubMed  Google Scholar 

  • Wilson PW, D'Agostino RB, Levy D, Belanger AM, Silbershatz H, Kannel WB (1998) Prediction of coronary heart disease using risk factor categories. Circulation 97:1837–1847

    Article  CAS  PubMed  Google Scholar 

  • Xu W, Qiu C, Gatz M, Pedersen NL, Johansson B, Fratiglioni L (2009) Mid- and late-life diabetes in relation to the risk of dementia: a population-based twin study. Diabetes 58:71–77

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yoshii F, Barker WW, Chang JY, Loewenstein D, Apicella A, Smith D et al (1988) Sensitivity of cerebral glucose metabolism to age, gender, brain volume, brain atrophy, and cerebrovascular risk factors. J Cereb Blood Flow Metab 8:654–661

    Article  CAS  PubMed  Google Scholar 

  • Zlokovic BV (2005) Neurovascular mechanisms of Alzheimer's neurodegeneration [Review]. Trends Neurosci 28:202–208

    Article  CAS  PubMed  Google Scholar 

  • Zlokovic BV (2010) Neurodegeneration and the neurovascular unit. Nat Med 16:1370–1371

    Article  CAS  PubMed  Google Scholar 

Further Readings

Download references

Acknowledgments

The authors thank Carlos Alberto Melo de Morais for helping with technical support, and Dr. Anna Maria Andrei for helping with cardiological evaluation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jaqueline Hatsuko Tamashiro-Duran.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 21 kb)

About this article

Cite this article

Tamashiro-Duran, J.H., Squarzoni, P., de Souza Duran, F.L. et al. Cardiovascular risk in cognitively preserved elderlies is associated with glucose hypometabolism in the posterior cingulate cortex and precuneus regardless of brain atrophy and apolipoprotein gene variations. AGE 35, 777–792 (2013). https://doi.org/10.1007/s11357-012-9413-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11357-012-9413-y

Keywords

Navigation