Skip to main content
Top
Published in: European Journal of Nuclear Medicine and Molecular Imaging 4/2014

01-04-2014 | Original Article

Plasma antioxidants and brain glucose metabolism in elderly subjects with cognitive complaints

Authors: Agnese Picco, M. Cristina Polidori, Michela Ferrara, Roberta Cecchetti, Dario Arnaldi, Mauro Baglioni, Silvia Morbelli, Patrizia Bastiani, Irene Bossert, Giuliana Fiorucci, Andrea Brugnolo, Massimo Eugenio Dottorini, Flavio Nobili, Patrizia Mecocci

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 4/2014

Login to get access

Abstract

Purpose

The role of oxidative stress is increasingly recognized in cognitive disorders of the elderly, notably Alzheimer’s disease (AD). In these subjects brain18F-FDG PET is regarded as a reliable biomarker of neurodegeneration. We hypothesized that oxidative stress could play a role in impairing brain glucose utilization in elderly subjects with increasing severity of cognitive disturbance.

Methods

The study group comprised 85 subjects with cognitive disturbance of increasing degrees of severity including 23 subjects with subjective cognitive impairment (SCI), 28 patients with mild cognitive impairment and 34 patients with mild AD. In all subjects brain FDG PET was performed and plasma activities of extracellular superoxide dismutase (eSOD), catalase and glutathione peroxidase were measured. Voxel-based analysis (SPM8) was used to compare FDG PET between groups and to evaluate correlations between plasma antioxidants and glucose metabolism in the whole group of subjects, correcting for age and Mini-Mental State Examination score.

Results

Brain glucose metabolism progressively decreased in the bilateral posterior temporoparietal and cingulate cortices across the three groups, from SCI to mild AD. eSOD activity was positively correlated with glucose metabolism in a large area of the left temporal lobe including the superior, middle and inferior temporal gyri and the fusiform gyrus.

Conclusion

These results suggest a role of oxidative stress in the impairment of glucose utilization in the left temporal lobe structures in elderly patients with cognitive abnormalities, including AD and conditions predisposing to AD. Further studies exploring the oxidative stress–energy metabolism axis are considered worthwhile in larger groups of these patients in order to identify pivotal pathophysiological mechanisms and innovative therapeutic opportunities.
Literature
1.
go back to reference Butterfield DA, Swomley AM, Sultana R. Amyloid β-peptide (1-42)-induced oxidative stress in Alzheimer disease: importance in disease pathogenesis and progression. Antioxid Redox Signal. 2013;19:823–35.PubMedCrossRef Butterfield DA, Swomley AM, Sultana R. Amyloid β-peptide (1-42)-induced oxidative stress in Alzheimer disease: importance in disease pathogenesis and progression. Antioxid Redox Signal. 2013;19:823–35.PubMedCrossRef
2.
go back to reference Smith MA, Nunomura A, Lee HG, Zhu X, Moreira PI, Avila J, et al. Chronological primacy of oxidative stress in Alzheimer’s disease. Neurobiol Aging. 2005;26:579–80.PubMedCrossRef Smith MA, Nunomura A, Lee HG, Zhu X, Moreira PI, Avila J, et al. Chronological primacy of oxidative stress in Alzheimer’s disease. Neurobiol Aging. 2005;26:579–80.PubMedCrossRef
3.
go back to reference Cadenas E. Mitochondrial free radical production and cell signaling. Mol Aspects Med. 2004;25:17–26.PubMedCrossRef Cadenas E. Mitochondrial free radical production and cell signaling. Mol Aspects Med. 2004;25:17–26.PubMedCrossRef
4.
5.
go back to reference Padurariu M, Ciobica A, Hritcu L, Stoica B, Bild W, Stefanescu C. Changes of some oxidative stress markers in the serum of patients with mild cognitive impairment and Alzheimer’s disease. Neurosci Lett. 2010;469:6–10.PubMedCrossRef Padurariu M, Ciobica A, Hritcu L, Stoica B, Bild W, Stefanescu C. Changes of some oxidative stress markers in the serum of patients with mild cognitive impairment and Alzheimer’s disease. Neurosci Lett. 2010;469:6–10.PubMedCrossRef
6.
go back to reference Sies H, Cadenas E. Oxidative stress: damage to intact cells and organs. Philos Trans R Soc Lond B Biol Sci. 1985;311:617–31.PubMedCrossRef Sies H, Cadenas E. Oxidative stress: damage to intact cells and organs. Philos Trans R Soc Lond B Biol Sci. 1985;311:617–31.PubMedCrossRef
7.
go back to reference Tamagno E, Parola M, Bardini P, Piccini A, Borghi R, Guglielmotto M, et al. Beta-site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways. J Neurochem. 2005;92:628–36.PubMedCrossRef Tamagno E, Parola M, Bardini P, Piccini A, Borghi R, Guglielmotto M, et al. Beta-site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways. J Neurochem. 2005;92:628–36.PubMedCrossRef
8.
go back to reference Tamagno E, Guglielmotto M, Aragno M, Borghi R, Autelli R, Giliberto L, et al. Oxidative stress activates a positive feedback between the gamma- and beta-secretase cleavages of the beta-amyloid precursor protein. J Neurochem. 2008;104:683–95.PubMedCentralPubMed Tamagno E, Guglielmotto M, Aragno M, Borghi R, Autelli R, Giliberto L, et al. Oxidative stress activates a positive feedback between the gamma- and beta-secretase cleavages of the beta-amyloid precursor protein. J Neurochem. 2008;104:683–95.PubMedCentralPubMed
9.
go back to reference Butterfield DA, Griffin S, Munch G, Pasinetti G. Amyloid beta-peptide and amyloid pathology are central to the oxidative stress and inflammatory cascades under which Alzheimer’s disease brain exists. J Alzheimers Dis. 2002;4:193–201.PubMed Butterfield DA, Griffin S, Munch G, Pasinetti G. Amyloid beta-peptide and amyloid pathology are central to the oxidative stress and inflammatory cascades under which Alzheimer’s disease brain exists. J Alzheimers Dis. 2002;4:193–201.PubMed
10.
go back to reference Behl C. Oxidative stress in Alzheimer’s disease: implications for prevention and therapy. Subcell Biochem. 2005;38:65–78.PubMedCrossRef Behl C. Oxidative stress in Alzheimer’s disease: implications for prevention and therapy. Subcell Biochem. 2005;38:65–78.PubMedCrossRef
11.
go back to reference Gòmez-Ramos A, Dìaz-Nido J, Smith MA, Perry G, Avila J. Effect of the lipid peroxidation product acrolein on tau phosphorylation in neural cells. J Neurosci Res. 2003;71:863–70.PubMedCrossRef Gòmez-Ramos A, Dìaz-Nido J, Smith MA, Perry G, Avila J. Effect of the lipid peroxidation product acrolein on tau phosphorylation in neural cells. J Neurosci Res. 2003;71:863–70.PubMedCrossRef
12.
go back to reference Zhu X, Rottkamp CA, Boux H, Takeda A, Perry G, Smith MA. Activation of p38 kinase links tau phosphorylation, oxidative stress, and cell cycle-related events in Alzheimer disease. J Neuropathol Exp Neurol. 2000;59:880–8.PubMed Zhu X, Rottkamp CA, Boux H, Takeda A, Perry G, Smith MA. Activation of p38 kinase links tau phosphorylation, oxidative stress, and cell cycle-related events in Alzheimer disease. J Neuropathol Exp Neurol. 2000;59:880–8.PubMed
13.
14.
go back to reference Mariani E, Polidori MC, Cherubini A, Mecocci P. Oxidative stress in brain aging, neurodegenerative and vascular diseases: an overview. J Chromatogr B Analyt Technol Biomed Life Sci. 2005;827:65–75.PubMedCrossRef Mariani E, Polidori MC, Cherubini A, Mecocci P. Oxidative stress in brain aging, neurodegenerative and vascular diseases: an overview. J Chromatogr B Analyt Technol Biomed Life Sci. 2005;827:65–75.PubMedCrossRef
15.
go back to reference Allaman I, Bélanger M, Magistretti PJ. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci. 2011;34:76–87.PubMedCrossRef Allaman I, Bélanger M, Magistretti PJ. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci. 2011;34:76–87.PubMedCrossRef
16.
go back to reference Massaad CA, Pautler RG, Klann E. Mitochondrial superoxide: a key player in Alzheimer’s disease. Aging (Albany NY). 2005;1:758–61. Massaad CA, Pautler RG, Klann E. Mitochondrial superoxide: a key player in Alzheimer’s disease. Aging (Albany NY). 2005;1:758–61.
18.
go back to reference Wahlund LO, Barkhof F, Fazekas F, Bronge L, Augustin M, Sjögren M, et al. European task force on age-related white matter changes. A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke. 2001;32:1318–22.PubMedCrossRef Wahlund LO, Barkhof F, Fazekas F, Bronge L, Augustin M, Sjögren M, et al. European task force on age-related white matter changes. A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke. 2001;32:1318–22.PubMedCrossRef
19.
go back to reference Katz S, Downs TD, Cash HR, Grotz RC. Progress in development of the index of ADL. Gerontologist. 1970;10:20–30.PubMedCrossRef Katz S, Downs TD, Cash HR, Grotz RC. Progress in development of the index of ADL. Gerontologist. 1970;10:20–30.PubMedCrossRef
20.
go back to reference Lawton MP, Brody EM. Assessment of older people; self maintaining and instrumental activities of daily living. Gerontologist. 1969;9:179–86.PubMedCrossRef Lawton MP, Brody EM. Assessment of older people; self maintaining and instrumental activities of daily living. Gerontologist. 1969;9:179–86.PubMedCrossRef
21.
go back to reference Folstein MF, Folstein SE, McHugh PR. “Mini-Mental State”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–98.PubMedCrossRef Folstein MF, Folstein SE, McHugh PR. “Mini-Mental State”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–98.PubMedCrossRef
22.
go back to reference McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack Jr CR, Kawas CH, 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;7:263–9.PubMedCentralPubMedCrossRef McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack Jr CR, Kawas CH, 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;7:263–9.PubMedCentralPubMedCrossRef
23.
go back to reference Loeb C, Gandolfo C. Diagnostic evaluation of degenerative and vascular dementia. Stroke. 1983;14:399–401.PubMedCrossRef Loeb C, Gandolfo C. Diagnostic evaluation of degenerative and vascular dementia. Stroke. 1983;14:399–401.PubMedCrossRef
24.
go back to reference Rey A. L’examenclinique en psychologie. Paris: Presses Universitaires de France; 1958. Rey A. L’examenclinique en psychologie. Paris: Presses Universitaires de France; 1958.
25.
go back to reference Novelli G, Papagno C, Capitani E, Laiacona M, Cappa SF. Tre test clinici di memoria verbale a lungo termine: taratura su soggetti normali. Arch Psicol Neurol Psichiatria. 2013;47:278–96. Novelli G, Papagno C, Capitani E, Laiacona M, Cappa SF. Tre test clinici di memoria verbale a lungo termine: taratura su soggetti normali. Arch Psicol Neurol Psichiatria. 2013;47:278–96.
26.
go back to reference Carlesimo GA, Caltagirone C, Gainotti G. The mental deterioration battery: normative data, diagnostic reliability and qualitative analysis of cognitive impairment. The group for the standardization of the mental deterioration battery. Eur Neurol. 1996;36:378–84.PubMedCrossRef Carlesimo GA, Caltagirone C, Gainotti G. The mental deterioration battery: normative data, diagnostic reliability and qualitative analysis of cognitive impairment. The group for the standardization of the mental deterioration battery. Eur Neurol. 1996;36:378–84.PubMedCrossRef
27.
28.
go back to reference L’Abbé MR, Fisher PWF. Automated assay of superoxide dismutase in blood. Methods Enzymol. 1990;186:232–7.PubMedCrossRef L’Abbé MR, Fisher PWF. Automated assay of superoxide dismutase in blood. Methods Enzymol. 1990;186:232–7.PubMedCrossRef
29.
go back to reference Sandström J, Nilsson P, Karlsson K, Marklund SL. 10-fold increase in human plasma extracellular superoxide dismutase content caused by a mutation in heparin-binding domain. J Biol Chem. 1994;269:19163–6.PubMed Sandström J, Nilsson P, Karlsson K, Marklund SL. 10-fold increase in human plasma extracellular superoxide dismutase content caused by a mutation in heparin-binding domain. J Biol Chem. 1994;269:19163–6.PubMed
30.
go back to reference Zhou LC, Xiang W, Potts J, Floyd M, Sharan C, Yang H, et al. Reduction in extracellular superoxide dismutase activity in African-American patients with hypertension. Free Radic Biol Med. 2006;41:1384–91.PubMedCrossRef Zhou LC, Xiang W, Potts J, Floyd M, Sharan C, Yang H, et al. Reduction in extracellular superoxide dismutase activity in African-American patients with hypertension. Free Radic Biol Med. 2006;41:1384–91.PubMedCrossRef
31.
32.
go back to reference Beers RF, Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem. 1952;195:133–40.PubMed Beers RF, Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem. 1952;195:133–40.PubMed
33.
go back to reference Varrone A, Asenbaum S, Vander Borght T, Booij J, Nobili F, Någren K, et al. EANM procedure guidelines for PET brain imaging using [18F]FDG, version 2. Eur J Nucl Med Mol Imaging. 2009;36:2103–10.PubMedCrossRef Varrone A, Asenbaum S, Vander Borght T, Booij J, Nobili F, Någren K, et al. EANM procedure guidelines for PET brain imaging using [18F]FDG, version 2. Eur J Nucl Med Mol Imaging. 2009;36:2103–10.PubMedCrossRef
34.
go back to reference Morbelli S, Drzezga A, Perneczky R, Frisoni GB, Caroli A, Van Berckel BN, et al. Resting metabolic connectivity in prodromal Alzheimer’s disease. A European Alzheimer Disease Consortium (EADC) project. Neurobiol Aging. 2012;33:2533–50.PubMedCrossRef Morbelli S, Drzezga A, Perneczky R, Frisoni GB, Caroli A, Van Berckel BN, et al. Resting metabolic connectivity in prodromal Alzheimer’s disease. A European Alzheimer Disease Consortium (EADC) project. Neurobiol Aging. 2012;33:2533–50.PubMedCrossRef
35.
go back to reference Gispert JD, Pascau J, Reig S, Martínez-Lázaro R, Molina V, García-Barreno P, et al. Influence of the normalization template on the outcome of statistical parametric mapping of PET scans. Neuroimage. 2003;19:601–12.PubMedCrossRef Gispert JD, Pascau J, Reig S, Martínez-Lázaro R, Molina V, García-Barreno P, et al. Influence of the normalization template on the outcome of statistical parametric mapping of PET scans. Neuroimage. 2003;19:601–12.PubMedCrossRef
36.
go back to reference Oishi N, Udaka F, Kameyama M, Sawamoto N, Hashikawa K, Fukuyama H. Regional cerebral blood flow in Parkinson disease with nonpsychotic visual hallucinations. Neurology. 2005;65:1708–15.PubMedCrossRef Oishi N, Udaka F, Kameyama M, Sawamoto N, Hashikawa K, Fukuyama H. Regional cerebral blood flow in Parkinson disease with nonpsychotic visual hallucinations. Neurology. 2005;65:1708–15.PubMedCrossRef
37.
go back to reference Rodriguez G, Morbelli S, Brugnolo A, Calvini P, Girtler N, Piccardo A, et al. Global cognitive impairment should be taken into account in SPECT-neuropsychology correlations: the example of verbal memory in very mild Alzheimer’s disease. Eur J Nucl Med Mol Imaging. 2005;32:1186–92.PubMedCrossRef Rodriguez G, Morbelli S, Brugnolo A, Calvini P, Girtler N, Piccardo A, et al. Global cognitive impairment should be taken into account in SPECT-neuropsychology correlations: the example of verbal memory in very mild Alzheimer’s disease. Eur J Nucl Med Mol Imaging. 2005;32:1186–92.PubMedCrossRef
38.
go back to reference Zelko IN, Mariani TJ, Folz RJ. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med. 2002;33:337–49.PubMedCrossRef Zelko IN, Mariani TJ, Folz RJ. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med. 2002;33:337–49.PubMedCrossRef
39.
go back to reference Tasaki H, Yamashita K, Tsutsui M, Kamezaki F, Kubara T, Tanaka S, et al. Heparin-released extracellular superoxide dismutase is reduced in patients with coronary artery atherosclerosis. Atherosclerosis. 2006;187:131–8.PubMedCrossRef Tasaki H, Yamashita K, Tsutsui M, Kamezaki F, Kubara T, Tanaka S, et al. Heparin-released extracellular superoxide dismutase is reduced in patients with coronary artery atherosclerosis. Atherosclerosis. 2006;187:131–8.PubMedCrossRef
40.
go back to reference De la Torre JC. Alzheimer’s disease: how does it start? J Alzheimers Dis. 2002;4:497–512.PubMed De la Torre JC. Alzheimer’s disease: how does it start? J Alzheimers Dis. 2002;4:497–512.PubMed
41.
go back to reference Polidori MC, Pientka L. Bridging the pathophysiology of Alzheimer’s disease with vascular pathology: the feed-back, the feed-forward, and oxidative stress. J Alzheimers Dis. 2012;28:1–9.PubMed Polidori MC, Pientka L. Bridging the pathophysiology of Alzheimer’s disease with vascular pathology: the feed-back, the feed-forward, and oxidative stress. J Alzheimers Dis. 2012;28:1–9.PubMed
42.
go back to reference Rinaldi P, Polidori MC, Metastasio A, Mariani E, Mattioli P, Cherubini A, et al. Plasma antioxidants are similarly depleted in mild cognitive impairment and in Alzheimer’s disease. Neurobiol Aging. 2003;24:915–9.PubMedCrossRef Rinaldi P, Polidori MC, Metastasio A, Mariani E, Mattioli P, Cherubini A, et al. Plasma antioxidants are similarly depleted in mild cognitive impairment and in Alzheimer’s disease. Neurobiol Aging. 2003;24:915–9.PubMedCrossRef
43.
go back to reference Baumbach GL, Didion SP, Faraci FM. Hypertrophy of cerebral arterioles in mice deficient in expression of the gene for CuZn superoxide dismutase. Stroke. 2006;37:1850–5.PubMedCrossRef Baumbach GL, Didion SP, Faraci FM. Hypertrophy of cerebral arterioles in mice deficient in expression of the gene for CuZn superoxide dismutase. Stroke. 2006;37:1850–5.PubMedCrossRef
44.
go back to reference Didion SP, Hathaway CA, Faraci FM. Superoxide levels and function of cerebral blood vessels after inhibition of CuZn-SOD. Am J Physiol Heart Circ Physiol. 2001;281:H1697–703.PubMed Didion SP, Hathaway CA, Faraci FM. Superoxide levels and function of cerebral blood vessels after inhibition of CuZn-SOD. Am J Physiol Heart Circ Physiol. 2001;281:H1697–703.PubMed
45.
go back to reference Yada T, Shimokawa H, Morikawa K, Takaki A, Shinozaki Y, Mori H, et al. Role of Cu, Zn-SOD in the synthesis of endogenous vasodilator hydrogen peroxide during reactive hyperemia in mouse mesenteric microcirculation in vivo. Am J Physiol Heart Circ Physiol. 2008;294:H441–8.PubMedCrossRef Yada T, Shimokawa H, Morikawa K, Takaki A, Shinozaki Y, Mori H, et al. Role of Cu, Zn-SOD in the synthesis of endogenous vasodilator hydrogen peroxide during reactive hyperemia in mouse mesenteric microcirculation in vivo. Am J Physiol Heart Circ Physiol. 2008;294:H441–8.PubMedCrossRef
46.
go back to reference Demchenko IT, Gutsaeva DR, Moskvin AN, Zhilyaev SY. Involvement of extracellular superoxide dismutase in regulating brain blood flow. Neurosci Behav Physiol. 2010;40:173–8.PubMedCrossRef Demchenko IT, Gutsaeva DR, Moskvin AN, Zhilyaev SY. Involvement of extracellular superoxide dismutase in regulating brain blood flow. Neurosci Behav Physiol. 2010;40:173–8.PubMedCrossRef
47.
go back to reference Federico A, Cardaioli E, Da Pozzo P, Formichi P, Gallus GN, Radi E. Mitochondria, oxidative stress and neurodegeneration. J Neurol Sci. 2012;322:254–62.PubMedCrossRef Federico A, Cardaioli E, Da Pozzo P, Formichi P, Gallus GN, Radi E. Mitochondria, oxidative stress and neurodegeneration. J Neurol Sci. 2012;322:254–62.PubMedCrossRef
48.
go back to reference Rajagopalan P, Toga AW, Jack CR, Weiner MW, Thompson PM. Fat-mass-related hormone, plasma leptin, predicts brain volumes in the elderly. Neuroreport. 2013;24:58–62.PubMedCentralPubMedCrossRef Rajagopalan P, Toga AW, Jack CR, Weiner MW, Thompson PM. Fat-mass-related hormone, plasma leptin, predicts brain volumes in the elderly. Neuroreport. 2013;24:58–62.PubMedCentralPubMedCrossRef
49.
go back to reference Toledo JB, Da X, Bhatt P, Wolk DA, Arnold SE, Shaw LM. Relationship between plasma analytes and SPARE-AD defined brain atrophy patterns in ADNI. PLoS One. 2013;8:e55531.PubMedCentralPubMedCrossRef Toledo JB, Da X, Bhatt P, Wolk DA, Arnold SE, Shaw LM. Relationship between plasma analytes and SPARE-AD defined brain atrophy patterns in ADNI. PLoS One. 2013;8:e55531.PubMedCentralPubMedCrossRef
50.
go back to reference den Heijer T, Vermeer SE, Clarke R, Oudkerk M, Koudstaal PJ, Hofman A, et al. Homocysteine and brain atrophy on MRI of non-demented elderly. Brain. 2003;126:170–5.CrossRef den Heijer T, Vermeer SE, Clarke R, Oudkerk M, Koudstaal PJ, Hofman A, et al. Homocysteine and brain atrophy on MRI of non-demented elderly. Brain. 2003;126:170–5.CrossRef
51.
go back to reference Terni B, Boada J, Portero-Otin M, Pamplona R, Ferrer I. Mitochondrial ATP-synthase in the entorhinal cortex is a target of oxidative stress at stages I/II of Alzheimer’s disease pathology. Brain Pathol. 2010;20:222–33.PubMedCrossRef Terni B, Boada J, Portero-Otin M, Pamplona R, Ferrer I. Mitochondrial ATP-synthase in the entorhinal cortex is a target of oxidative stress at stages I/II of Alzheimer’s disease pathology. Brain Pathol. 2010;20:222–33.PubMedCrossRef
52.
go back to reference Limón ID, Díaz A, Mendieta L, Chamorro G, Espinosa B, Zenteno E, et al. Amyloid-beta(25-35) impairs memory and increases NO in the temporal cortex of rats. Neurosci Res. 2009;63:129–37.PubMedCrossRef Limón ID, Díaz A, Mendieta L, Chamorro G, Espinosa B, Zenteno E, et al. Amyloid-beta(25-35) impairs memory and increases NO in the temporal cortex of rats. Neurosci Res. 2009;63:129–37.PubMedCrossRef
53.
go back to reference Wang J, Xiong S, Xie C, Markesbery WR. Increased oxidative damage in nuclear and mitochondrial DNA in Alzheimer’s disease. J Neurochem. 2005;93:953–62.PubMedCrossRef Wang J, Xiong S, Xie C, Markesbery WR. Increased oxidative damage in nuclear and mitochondrial DNA in Alzheimer’s disease. J Neurochem. 2005;93:953–62.PubMedCrossRef
54.
go back to reference Sultana R, Butterfield DA. Oxidatively modified, mitochondria-relevant brain proteins in subjects with Alzheimer disease and mild cognitive impairment. J Bioenerg Biomembr. 2009;41:441–6.PubMedCentralPubMedCrossRef Sultana R, Butterfield DA. Oxidatively modified, mitochondria-relevant brain proteins in subjects with Alzheimer disease and mild cognitive impairment. J Bioenerg Biomembr. 2009;41:441–6.PubMedCentralPubMedCrossRef
55.
go back to reference Hovorkova P, Kristofikova Z, Horinek A, Ripova D, Majer E, Zach P, et al. Lateralization of 17beta-hydroxysteroid dehydrogenase type 10 in hippocampi of demented and psychotic people. Dement Geriatr Cogn Disord. 2008;26:193–8.PubMedCrossRef Hovorkova P, Kristofikova Z, Horinek A, Ripova D, Majer E, Zach P, et al. Lateralization of 17beta-hydroxysteroid dehydrogenase type 10 in hippocampi of demented and psychotic people. Dement Geriatr Cogn Disord. 2008;26:193–8.PubMedCrossRef
57.
go back to reference Morbelli S, Piccardo A, Villavecchia G, Dessi B, Brugnolo A, Piccini A, et al. Mapping brain morphological and functional conversion patterns in amnestic MCI: a voxel-based MRI and FDG-PET study. Eur J Nucl Med Mol Imaging. 2010;37:36–45.PubMedCrossRef Morbelli S, Piccardo A, Villavecchia G, Dessi B, Brugnolo A, Piccini A, et al. Mapping brain morphological and functional conversion patterns in amnestic MCI: a voxel-based MRI and FDG-PET study. Eur J Nucl Med Mol Imaging. 2010;37:36–45.PubMedCrossRef
58.
go back to reference Bozzali M, Padovani A, Caltagirone C, Borroni B. Regional grey matter loss and brain disconnection across Alzheimer disease evolution. Curr Med Chem. 2011;18:2452–8.PubMedCrossRef Bozzali M, Padovani A, Caltagirone C, Borroni B. Regional grey matter loss and brain disconnection across Alzheimer disease evolution. Curr Med Chem. 2011;18:2452–8.PubMedCrossRef
59.
go back to reference Bozoki AC, Korolev IO, Davis NC, Hoisington LA, Berger KL. Disruption of limbic white matter pathways in mild cognitive impairment and Alzheimer’s disease: a DTI/FDG-PET study. Hum Brain Mapp. 2012;33:1792–802.PubMedCrossRef Bozoki AC, Korolev IO, Davis NC, Hoisington LA, Berger KL. Disruption of limbic white matter pathways in mild cognitive impairment and Alzheimer’s disease: a DTI/FDG-PET study. Hum Brain Mapp. 2012;33:1792–802.PubMedCrossRef
60.
go back to reference Grimmer T, Faust M, Auer F, Alexopoulos P, Förstl H, Henriksen G, et al. White matter hyperintensities predict amyloid increase in Alzheimer’s disease. Neurobiol Aging. 2012;33:2766–73.PubMedCrossRef Grimmer T, Faust M, Auer F, Alexopoulos P, Förstl H, Henriksen G, et al. White matter hyperintensities predict amyloid increase in Alzheimer’s disease. Neurobiol Aging. 2012;33:2766–73.PubMedCrossRef
61.
go back to reference Clausen A, Xu X, Bi X, Baudry M. Effects of the superoxide dismutase/catalase mimetic EUK-207 in a mouse model of Alzheimer’s disease: protection against and interruption of progression of amyloid and tau pathology and cognitive decline. J Alzheimers Dis. 2012;30:183–208.PubMed Clausen A, Xu X, Bi X, Baudry M. Effects of the superoxide dismutase/catalase mimetic EUK-207 in a mouse model of Alzheimer’s disease: protection against and interruption of progression of amyloid and tau pathology and cognitive decline. J Alzheimers Dis. 2012;30:183–208.PubMed
Metadata
Title
Plasma antioxidants and brain glucose metabolism in elderly subjects with cognitive complaints
Authors
Agnese Picco
M. Cristina Polidori
Michela Ferrara
Roberta Cecchetti
Dario Arnaldi
Mauro Baglioni
Silvia Morbelli
Patrizia Bastiani
Irene Bossert
Giuliana Fiorucci
Andrea Brugnolo
Massimo Eugenio Dottorini
Flavio Nobili
Patrizia Mecocci
Publication date
01-04-2014
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 4/2014
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-013-2638-x

Other articles of this Issue 4/2014

European Journal of Nuclear Medicine and Molecular Imaging 4/2014 Go to the issue