A cross-sectional comparison of brain glucose and ketone metabolism in cognitively healthy older adults, mild cognitive impairment and early Alzheimer's disease

Experimental Gerontology

Volumn 107, Issue , 2018, Pages 18-26

  Croteau, E ^a   Castellano, C A ^a   Fortier, M ^a   Bocti, C ^a   Fulop, T ^a   Paquet, N ^a,b   Cunnane, S C ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b CENTRE HOSPITALIER UNIVERSITAIRE DE SHERBROOKE   (Canada)

Author keywords

Acetoacetate; Alzheimer's disease (AD); Brain metabolism; Glucose; Ketones; Mild cognitive impairment (MCI)

Indexed keywords

ACETOACETIC ACID; GLUCOSE; ACETOACETIC ACID DERIVATIVE; FLUORODEOXYGLUCOSE F 18;

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN ATROPHY; BRAIN METABOLISM; BRAIN SIZE; CINGULATE GYRUS; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); CROSS-SECTIONAL STUDY; DISORDERS OF CARBOHYDRATE METABOLISM; ENERGY METABOLISM; FEMALE; FRONTAL LOBE; GLUCOSE METABOLISM; GRAY MATTER; HUMAN; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL LOBE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; SUBCORTEX; TEMPORAL CORTEX; TEMPORAL LOBE; BRAIN; CASE CONTROL STUDY; COGNITIVE DEFECT; COMPARATIVE STUDY; DIAGNOSTIC IMAGING; METABOLISM; STATISTICAL MODEL; VERY ELDERLY;

ACETOACETATES; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BRAIN; CASE-CONTROL STUDIES; COGNITIVE DYSFUNCTION; CROSS-SECTIONAL STUDIES; ENERGY METABOLISM; FEMALE; FLUORODEOXYGLUCOSE F18; GLUCOSE; HUMANS; LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE; POSITRON-EMISSION TOMOGRAPHY;

EID: 85025116229     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2017.07.004     Document Type: Article

References (37)

1. Ashraf, A., Fan, Z., Brooks, D.J., Edison, P., Cortical hypermetabolism in MCI subjects: a compensatory mechanism?. Eur. J. Nucl. Med. Mol. Imaging 42 (2015), 447–458.
2. Bailly, M., Destrieux, C., Hommet, C., Mondon, K., Cottier, J.P., Beaufils, E., Vierron, E., Vercouillie, J., Ibazizene, M., Voisin, T., Payoux, P., Barre, L., Camus, V., Guilloteau, D., Ribeiro, M.J., Precuneus and cingulate cortex atrophy and Hypometabolism in patients with Alzheimer's disease and mild cognitive impairment: MRI and (18)F-FDG PET quantitative analysis using FreeSurfer. Biomed. Res. Int., 583931, 2015, 2015.
3. Blomqvist, G., Thorell, J.O., Ingvar, M., Grill, V., Widen, L., Stone-Elander, S., Use of R-beta-[1-11C]hydroxybutyrate in PET studies of regional cerebral uptake of ketone bodies in humans. Am. J. Physiol. 269 (1995), E948–E959.
4. Brown, R.K., Bohnen, N.I., Wong, K.K., Minoshima, S., Frey, K.A., Brain PET in suspected dementia: patterns of altered FDG metabolism. Radiographics 34 (2014), 684–701.
5. Cahill, G.F. Jr., Fuel metabolism in starvation. Annu. Rev. Nutr. 26 (2006), 1–22.
6. Castellano, C.A., Nugent, S., Paquet, N., Tremblay, S., Bocti, C., Lacombe, G., Imbeault, H., Turcotte, E., Fulop, T., Cunnane, S.C., Lower brain 18F-fluorodeoxyglucose uptake but normal 11C-acetoacetate metabolism in mild Alzheimer's disease dementia. J. Alzheimers Dis. 43 (2015), 1343–1353.
7. Castellano, C.A., Paquet, N., Dionne, I.J., Imbeault, H., Langlois, F., Croteau, E., Tremblay, S., Fortier, M., Matte, J.J., Lacombe, G., Fulop, T., Bocti, C., Cunnane, S.C., A 3-Month aerobic training program improves brain energy metabolism in mild alzheimer's disease: preliminary results from a neuroimaging study. J. Alzheimers Dis., 2017.
8. Courchesne-Loyer, A., Fortier, M., Tremblay-Mercier, J., Chouinard-Watkins, R., Roy, M., Nugent, S., Castellano, C.A., Cunnane, S.C., Stimulation of mild, sustained ketonemia by medium-chain triacylglycerols in healthy humans: estimated potential contribution to brain energy metabolism. Nutrition 29 (2013), 635–640 (Burbank, Los Angeles County, Calif).
9. Courchesne-Loyer, A., Croteau, E., Castellano, C.A., St-Pierre, V., Hennebelle, M., Cunnane, S.C., Inverse relationship between brain glucose and ketone metabolism in adults during short-term moderate dietary ketosis: a dual tracer quantitative positron emission tomography study. J Cereb Blood Flow Metab, 2016.
10. Cunnane, S.C., Courchesne-Loyer, A., St-Pierre, V., Vandenberghe, C., Pierotti, T., Fortier, M., Croteau, E., Castellano, C.A., Can ketones compensate for deteriorating brain glucose uptake during aging?. Ann. N. Y. Acad. Sci. 1367 (2016), 12–20.
11. Cunnane, S.C., Courchesne-Loyer, A., Vandenberghe, C., St-Pierre, V., Fortier, M., Hennebelle, M., Croteau, E., Bocti, C., Fulop, T., Castellano, C.A., Can ketones help rescue brain fuel supply in later life? Implications for cognitive health during aging and the treatment of Alzheimer's disease. Front. Mol. Neurosci., 9, 2016, 53.
12. Del Sole, A., Clerici, F., Chiti, A., Lecchi, M., Mariani, C., Maggiore, L., Mosconi, L., Lucignani, G., Individual cerebral metabolic deficits in Alzheimer's disease and amnestic mild cognitive impairment: an FDG PET study. Eur. J. Nucl. Med. Mol. Imaging 35 (2008), 1357–1366.
13. Du, A.T., Schuff, N., Kramer, J.H., Rosen, H.J., Gorno-Tempini, M.L., Rankin, K., Miller, B.L., Weiner, M.W., Different regional patterns of cortical thinning in Alzheimer's disease and frontotemporal dementia. Brain 130 (2007), 1159–1166.
14. Dukart, J., Kherif, F., Mueller, K., Adaszewski, S., Schroeter, M.L., Frackowiak, R.S., Draganski, B., Generative FDG-PET and MRI model of aging and disease progression in Alzheimer's disease. PLoS Comput. Biol., 9, 2013, e1002987.
15. Gauthier, S., Reisberg, B., Zaudig, M., Petersen, R.C., Ritchie, K., Broich, K., Belleville, S., Brodaty, H., Bennett, D., Chertkow, H., Cummings, J.L., de Leon, M., Feldman, H., Ganguli, M., Hampel, H., Scheltens, P., Tierney, M.C., Whitehouse, P., Winblad, B., Mild cognitive impairment. Lancet 367 (2006), 1262–1270.
16. Hansen, T.I., Brezova, V., Eikenes, L., Haberg, A., Vangberg, T.R., How does the accuracy of intracranial volume measurements affect normalized brain volumes? Sample size estimates based on 966 subjects from the HUNT MRI cohort. AJNR Am. J. Neuroradiol. 36 (2015), 1450–1456.
17. Hebert, R., Carrier, R., Bilodeau, A., The functional autonomy measurement system (SMAF): description and validation of an instrument for the measurement of handicaps. Age Ageing 17 (1988), 293–302.
18. Jagust, W.J., Bandy, D., Chen, K., Foster, N.L., Landau, S.M., Mathis, C.A., Price, J.C., Reiman, E.M., Skovronsky, D., Koeppe, R.A., The Alzheimer's disease neuroimaging initiative positron emission tomography core. Alzheimers Dement. 6 (2010), 221–229.
19. Jagust, W.J., Landau, S.M., Koeppe, R.A., Reiman, E.M., Chen, K., Mathis, C.A., Price, J.C., Foster, N.L., Wang, A.Y., The Alzheimer's disease neuroimaging initiative 2 PET Core: 2015. Alzheimers Dement. 11 (2015), 757–771.
20. Jicha, G.A., Abner, E., Schmitt, F.A., Cooper, G.E., Stiles, N., Hamon, R., Carr, S., Smith, C.D., Markesbery, W.R., Clinical features of mild cognitive impairment differ in the research and tertiary clinic settings. Dement. Geriatr. Cogn. Disord. 26 (2008), 187–192.
21. Lacalle-Aurioles, M., Mateos-Perez, J.M., Guzman-De-Villoria, J.A., Olazaran, J., Cruz-Orduna, I., Aleman-Gomez, Y., Martino, M.E., Desco, M., Cerebral blood flow is an earlier indicator of perfusion abnormalities than cerebral blood volume in Alzheimer's disease. J. Cereb. Blood Flow Metab. 34 (2014), 654–659.
22. Logan, J., Graphical analysis of PET data applied to reversible and irreversible tracers. Nucl. Med. Biol. 27 (2000), 661–670.
23. Lying-Tunell, U., Lindblad, B.S., Malmlund, H.O., Persson, B., Cerebral blood flow and metabolic rate of oxygen, glucose, lactate, pyruvate, ketone bodies and amino acids. Acta Neurol. Scand. 63 (1981), 337–350.
24. McKhann, G.M., Knopman, D.S., Chertkow, H., Hyman, B.T., Jack, C.R. Jr., Kawas, C.H., Klunk, W.E., Koroshetz, W.J., Manly, J.J., Mayeux, R., Mohs, R.C., Morris, J.C., Rossor, M.N., Scheltens, P., Carrillo, M.C., Thies, B., Weintraub, S., Phelps, C.H., 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. 7 (2011), 263–269.
25. Minoshima, S., Giordani, B., Berent, S., Frey, K.A., Foster, N.L., Kuhl, D.E., Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann. Neurol. 42 (1997), 85–94.
26. Mosconi, L., Tsui, W.H., De Santi, S., Li, J., Rusinek, H., Convit, A., Li, Y., Boppana, M., de Leon, M.J., Reduced hippocampal metabolism in MCI and AD: automated FDG-PET image analysis. Neurology 64 (2005), 1860–1867.
27. Mosconi, L., Tsui, W.H., Herholz, K., Pupi, A., Drzezga, A., Lucignani, G., Reiman, E.M., Holthoff, V., Kalbe, E., Sorbi, S., Diehl-Schmid, J., Perneczky, R., Clerici, F., Caselli, R., Beuthien-Baumann, B., Kurz, A., Minoshima, S., de Leon, M.J., Multicenter standardized 18F-FDG PET diagnosis of mild cognitive impairment, Alzheimer's disease, and other dementias. J. Nucl. Med. 49 (2008), 390–398.
28. Mosconi, L., Mistur, R., Switalski, R., Tsui, W.H., Glodzik, L., Li, Y., Pirraglia, E., De Santi, S., Reisberg, B., Wisniewski, T., de Leon, M.J., FDG-PET changes in brain glucose metabolism from normal cognition to pathologically verified Alzheimer's disease. Eur. J. Nucl. Med. Mol. Imaging 36 (2009), 811–822.
29. Nugent, S., Tremblay, S., Chen, K.W., Ayutyanont, N., Roontiva, A., Castellano, C.A., Fortier, M., Roy, M., Courchesne-Loyer, A., Bocti, C., Lepage, M., Turcotte, E., Fulop, T., Reiman, E.M., Cunnane, S.C., Brain glucose and acetoacetate metabolism: a comparison of young and older adults. Neurobiol. Aging 35 (2014), 1386–1395.
30. Ogawa, M., Fukuyama, H., Ouchi, Y., Yamauchi, H., Kimura, J., Altered energy metabolism in Alzheimer's disease. J. Neurol. Sci. 139 (1996), 78–82.
31. Osorio, R.S., Berti, V., Mosconi, L., Li, Y., Glodzik, L., De Santi, S., de Leon, M.J., Evaluation of Early Dementia (Mild Cognitive Impairment). PET Clin, 5, 2010, 15–31.
32. Pagani, M., De Carli, F., Morbelli, S., Oberg, J., Chincarini, A., Frisoni, G.B., Galluzzi, S., Perneczky, R., Drzezga, A., van Berckel, B.N., Ossenkoppele, R., Didic, M., Guedj, E., Brugnolo, A., Picco, A., Arnaldi, D., Ferrara, M., Buschiazzo, A., Sambuceti, G., Nobili, F., Volume of interest-based [18F]fluorodeoxyglucose PET discriminates MCI converting to Alzheimer's disease from healthy controls. A European Alzheimer's disease consortium (EADC) study. Neuroimage Clin, 7, 2015, 34–42.
33. Petersen, R.C., Mild cognitive impairment as a diagnostic entity. J. Intern. Med. 256 (2004), 183–194.
34. Pfefferbaum, A., Rohlfing, T., Rosenbloom, M.J., Sullivan, E.V., Combining atlas-based parcellation of regional brain data acquired across scanners at 1.5 T and 3.0 T field strengths. Neuroimage 60 (2012), 940–951.
35. Vandenberghe, C., St-Pierre, V., Pierotti, T., Fortier, M., Castellano, C.A., Cunnane, S.C., Tricaprylin alone increases plasma ketone response more than coconut oil or other medium-chain triglycerides: an acute crossover study in healthy adults. Current developments in nutrition, 1, 2017, 1–5.
36. Verclytte, S., Lopes, R., Lenfant, P., Rollin, A., Semah, F., Leclerc, X., Pasquier, F., Delmaire, C., Cerebral Hypoperfusion and Hypometabolism detected by arterial spin labeling MRI and FDG-PET in early-onset Alzheimer's disease. J. Neuroimaging 26 (2016), 207–212.
37. Vriens, D., de Geus-Oei, L.F., Oyen, W.J., Visser, E.P., A curve-fitting approach to estimate the arterial plasma input function for the assessment of glucose metabolic rate and response to treatment. J. Nucl. Med. 50 (2009), 1933–1939.