User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Fluorodeoxyglucose metabolism associated with tau-amyloid interaction predicts memory decline : Tau, Amyloid, FDG, and Memory in Normal Aging

Primary tabs

download
  • Open access
  • PDF
  • 0.99 M
Hanseeuw, Bernard [UCL] Betensky, Rebecca A. Schultz, Aaron P. Papp, Kathryn V. Mormino, Elizabeth C. Johnson, Keith A.

(eng) OBJECTIVE: The aim of this article was to evaluate in normal older adults and preclinical Alzheimer's disease (AD) the impact of amyloid and regional tauopathy on cerebral glucose metabolism and subsequent memory decline. METHODS: We acquired positron emission tomography using F18 flortaucipir (tau), C11 Pittsburgh compound B (amyloid), and F18 fluorodeoxyglucose (FDG) in 90 clinically normal elderly of the Harvard Aging Brain Study. RESULTS: Posterior cingulate metabolism decreased when both amyloid and neocortical tau were high and predicted subsequent memory decline in a larger sample of normal elderly. In contrast, frontal hypometabolism related to the common age-related entorhinal tauopathy, but this dysfunction was independent of amyloid, and did not predict significant memory decline. Neocortical tauopathy was positively associated with metabolism in individuals with subthreshold amyloid, suggesting that glucose metabolism increases before decreasing in the course of preclinical AD. INTERPRETATION: Our study identified a synergistic effect of amyloid and tau deposits and demonstrated, for the first time, in normal elderly its link to AD-like hypometabolism and to AD-like memory decline. The amyloid effect was observed with tau in neocortex, but not with tau in entorhinal cortex, which is the common site of age-related tauopathy. Entorhinal tau was associated with frontal hypometabolism, but this dysfunction was not associated with memory loss

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès mixte
Publication date 2017
Language Anglais
Journal information "Annals of Neurology" - Vol. 81, no. 4, p. 583-596 (2017)
Peer reviewed yes
Publisher Wiley-Blackwell ((United States) New York, NY)
issn 0364-5134
e-issn 1531-8249
Publication status Publié
Affiliations UCL - SSS/IONS/NEUR - Clinical Neuroscience
UCL - (SLuc) Service de neurologie
Keywords Neurology ; Clinical Neurology
Links
  1. Nelson Peter T., Alafuzoff Irina, Bigio Eileen H., Bouras Constantin, Braak Heiko, Cairns Nigel J., Castellani Rudolph J., Crain Barbara J., Davies Peter, Tredici Kelly Del, Duyckaerts Charles, Frosch Matthew P., Haroutunian Vahram, Hof Patrick R., Hulette Christine M., Hyman Bradley T., Iwatsubo Takeshi, Jellinger Kurt A., Jicha Gregory A., Kövari Enikö, Kukull Walter A., Leverenz James B., Love Seth, Mackenzie Ian R., Mann David M., Masliah Eliezer, McKee Ann C., Montine Thomas J., Morris John C., Schneider Julie A., Sonnen Joshua A., Thal Dietmar R., Trojanowski John Q., Troncoso Juan C., Wisniewski Thomas, Woltjer Randall L., Beach Thomas G., Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature, 10.1097/nen.0b013e31825018f7
  2. Braak Heiko, Alafuzoff Irina, Arzberger Thomas, Kretzschmar Hans, Del Tredici Kelly, Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry, 10.1007/s00401-006-0127-z
  3. Price Joseph L., McKeel Daniel W., Buckles Virginia D., Roe Catherine M., Xiong Chengjie, Grundman Michael, Hansen Lawrence A., Petersen Ronald C., Parisi Joseph E., Dickson Dennis W., Smith Charles D., Davis Daron G., Schmitt Frederick A., Markesbery William R., Kaye Jeffrey, Kurlan Roger, Hulette Christine, Kurland Brenda F., Higdon Roger, Kukull Walter, Morris John C., Neuropathology of nondemented aging: Presumptive evidence for preclinical Alzheimer disease, 10.1016/j.neurobiolaging.2009.04.002
  4. Hyman Bradley T., Phelps Creighton H., Beach Thomas G., Bigio Eileen H., Cairns Nigel J., Carrillo Maria C., Dickson Dennis W., Duyckaerts Charles, Frosch Matthew P., Masliah Eliezer, Mirra Suzanne S., Nelson Peter T., Schneider Julie A., Thal Dietmar Rudolf, Thies Bill, Trojanowski John Q., Vinters Harry V., Montine Thomas J., National Institute on Aging–Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease, 10.1016/j.jalz.2011.10.007
  5. McKhann Guy M., Knopman David S., Chertkow Howard, Hyman Bradley T., Jack Clifford R., Kawas Claudia H., Klunk William E., Koroshetz Walter J., Manly Jennifer J., Mayeux Richard, Mohs Richard C., Morris John C., Rossor Martin N., Scheltens Philip, Carrillo Maria C., Thies Bill, Weintraub Sandra, Phelps Creighton 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, 10.1016/j.jalz.2011.03.005
  6. Chien, J Alzheimers Dis, 34, 457 (2013)
  7. Marquié Marta, Normandin Marc D., Vanderburg Charles R., Costantino Isabel M., Bien Elizabeth A., Rycyna Lisa G., Klunk William E., Mathis Chester A., Ikonomovic Milos D., Debnath Manik L., Vasdev Neil, Dickerson Bradford C., Gomperts Stephen N., Growdon John H., Johnson Keith A., Frosch Matthew P., Hyman Bradley T., Gómez-Isla Teresa, Validating novel tau positron emission tomography tracer [F-18]-AV-1451 (T807) on postmortem brain tissue : Validation of PET Tracer, 10.1002/ana.24517
  8. Johnson Keith A., Schultz Aaron, Betensky Rebecca A., Becker J. Alex, Sepulcre Jorge, Rentz Dorene, Mormino Elizabeth, Chhatwal Jasmeer, Amariglio Rebecca, Papp Kate, Marshall Gad, Albers Mark, Mauro Samantha, Pepin Lesley, Alverio Jonathan, Judge Kelly, Philiossaint Marlie, Shoup Timothy, Yokell Daniel, Dickerson Bradford, Gomez-Isla Teresa, Hyman Bradley, Vasdev Neil, Sperling Reisa, Tau positron emission tomographic imaging in aging and early Alzheimer disease : Tau PET in Aging and Early AD, 10.1002/ana.24546
  9. Schöll Michael, Lockhart Samuel N., Schonhaut Daniel R., O’Neil James P., Janabi Mustafa, Ossenkoppele Rik, Baker Suzanne L., Vogel Jacob W., Faria Jamie, Schwimmer Henry D., Rabinovici Gil D., Jagust William J., PET Imaging of Tau Deposition in the Aging Human Brain, 10.1016/j.neuron.2016.01.028
  10. Schwarz Adam J., Yu Peng, Miller Bradley B., Shcherbinin Sergey, Dickson James, Navitsky Michael, Joshi Abhinay D., Devous Michael D., Mintun Mark S., Regional profiles of the candidate tau PET ligand18F-AV-1451 recapitulate key features of Braak histopathological stages, 10.1093/brain/aww023
  11. Sepulcre J., Schultz A. P., Sabuncu M., Gomez-Isla T., Chhatwal J., Becker A., Sperling R., Johnson K. A., In Vivo Tau, Amyloid, and Gray Matter Profiles in the Aging Brain, 10.1523/jneurosci.0639-16.2016
  12. Foster N. L., Chase T. N., Fedio P., Patronas N. J., Brooks R. A., Chiro G. D., Alzheimer's disease: Focal cortical changes shown by positron emission tomography, 10.1212/wnl.33.8.961
  13. Friedland Robert P., Budinger Thomas F., Ganz Edward, Yano Yukio, Mathis Chester A., Koss Betty, Ober Beth A., Huesman Ronald H., Derenzo Steven E., Regional Cerebral Metabolic Alterations in Dementia of the Alzheimer Type : Positron Emission Tomography with [1818] Fluorodeoxyglucose, 10.1097/00004728-198308000-00003
  14. Minoshima Saroshi, Giordani Bruno, Berent Stanley, Frey Kirk A., Foster Norman L., Kuhl David E., Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease, 10.1002/ana.410420114
  15. Grober Ellen, Buschke Herman, Genuine memory deficits in dementia, 10.1080/87565648709540361
  16. Rousset Elodie, Harel Josée, Dubreuil Daniel J, Binding characteristics ofEscherichia colienterotoxin b (STb) to the pig jejunum and partial characterization of the molecule involved, 10.1006/mpat.1997.0193
  17. Greve Douglas N., Salat David H., Bowen Spencer L., Izquierdo-Garcia David, Schultz Aaron P., Catana Ciprian, Becker J. Alex, Svarer Claus, Knudsen Gitte M., Sperling Reisa A., Johnson Keith A., Different partial volume correction methods lead to different conclusions: An 18 F-FDG-PET study of aging, 10.1016/j.neuroimage.2016.02.042
  18. Müller-Gärtner Hans W., Links Jonathan M., Prince Jerry L., Bryan R. Nick, McVeigh Elliot, Leal Jeffrey P., Davatzikos Christos, Frost J. James, Measurement of Radiotracer Concentration in Brain Gray Matter Using Positron Emission Tomography: MRI-Based Correction for Partial Volume Effects, 10.1038/jcbfm.1992.81
  19. Mormino E. C., Betensky R. A., Hedden T., Schultz A. P., Ward A., Huijbers W., Rentz D. M., Johnson K. A., Sperling R. A., , Amyloid and APOE  4 interact to influence short-term decline in preclinical Alzheimer disease, 10.1212/wnl.0000000000000431
  20. Hoffman, J Nucl Med, 41, 1920 (2000)
  21. Sarazin M., Berr C., De Rotrou J., Fabrigoule C., Pasquier F., Legrain S., Michel B., Puel M., Volteau M., Touchon J., Verny M., Dubois B., Amnestic syndrome of the medial temporal type identifies prodromal AD: A longitudinal study, 10.1212/01.wnl.0000279336.36610.f7
  22. Wagner M., Wolf S., Reischies F. M., Daerr M., Wolfsgruber S., Jessen F., Popp J., Maier W., Hull M., Frolich L., Hampel H., Perneczky R., Peters O., Jahn H., Luckhaus C., Gertz H.- J., Schroder J., Pantel J., Lewczuk P., Kornhuber J., Wiltfang J., Biomarker validation of a cued recall memory deficit in prodromal Alzheimer disease, 10.1212/wnl.0b013e318245f447
  23. Chiaravalloti, Nucl Med Commun, 36, 461 (2015)
  24. Dowling N. Maritza, Johnson Sterling C., Gleason Carey E., Jagust William J., The mediational effects of FDG hypometabolism on the association between cerebrospinal fluid biomarkers and neurocognitive function, 10.1016/j.neuroimage.2014.10.050
  25. Alexopoulos Panagiotis, Kriett Laura, Haller Bernhard, Klupp Elisabeth, Gray Katherine, Grimmer Timo, Laskaris Nikolaos, Förster Stefan, Perneczky Robert, Kurz Alexander, Drzezga Alexander, Fellgiebel Andreas, Yakushev Igor, Limited agreement between biomarkers of neuronal injury at different stages of Alzheimer's disease, 10.1016/j.jalz.2014.03.006
  26. Yakushev Igor, J. Muller Matthias, Buchholz Hans-Georg, Lang Ulrike, Rossmann Heidi, Hampel Harald, Schreckenberger Mathias, Fellgiebel Andreas, Stage-Dependent Agreement between Cerebrospinal Fluid Proteins and FDG-PET Findings in Alzheimer's Disease, 10.2174/156720512799361592
  27. Landau Susan M., Mintun Mark A., Joshi Abhinay D., Koeppe Robert A., Petersen Ronald C., Aisen Paul S., Weiner Michael W., Jagust William J., , Amyloid deposition, hypometabolism, and longitudinal cognitive decline, 10.1002/ana.23650
  28. Jagust William J., Landau Susan M., Koeppe Robert A., Reiman Eric M., Chen Kewei, Mathis Chester A., Price Julie C., Foster Norman L., Wang Angela Y., The Alzheimer's Disease Neuroimaging Initiative 2 PET Core: 2015, 10.1016/j.jalz.2015.05.001
  29. DeCarli, Neurodegeneration, 1, 113 (1991)
  30. Petrie Eric C., Cross Donna J., Galasko Douglas, Schellenberg Gerard D., Raskind Murray A., Peskind Elaine R., Minoshima Satoshi, Preclinical Evidence of Alzheimer Changes : Convergent Cerebrospinal Fluid Biomarker and Fluorodeoxyglucose Positron Emission Tomography Findings, 10.1001/archneurol.2009.59
  31. Minoshima Satoshi, Imaging Alzheimer's disease: clinical applications, 10.1016/s1052-5149(03)00099-6
  32. Hanseeuw Bernard J., Schultz Aaron P., Betensky Rebecca A., Sperling Reisa A., Johnson Keith A., Decreased hippocampal metabolism in high-amyloid mild cognitive impairment, 10.1016/j.jalz.2016.06.2357
  33. Ossenkoppele Rik, Schonhaut Daniel R., Schöll Michael, Lockhart Samuel N., Ayakta Nagehan, Baker Suzanne L., O’Neil James P., Janabi Mustafa, Lazaris Andreas, Cantwell Averill, Vogel Jacob, Santos Miguel, Miller Zachary A., Bettcher Brianne M., Vossel Keith A., Kramer Joel H., Gorno-Tempini Maria L., Miller Bruce L., Jagust William J., Rabinovici Gil D., Tau PET patterns mirror clinical and neuroanatomical variability in Alzheimer’s disease, 10.1093/brain/aww027
  34. Benzinger T. L. S., Blazey T., Jack C. R., Koeppe R. A., Su Y., Xiong C., Raichle M. E., Snyder A. Z., Ances B. M., Bateman R. J., Cairns N. J., Fagan A. M., Goate A., Marcus D. S., Aisen P. S., Christensen J. J., Ercole L., Hornbeck R. C., Farrar A. M., Aldea P., Jasielec M. S., Owen C. J., Xie X., Mayeux R., Brickman A., McDade E., Klunk W., Mathis C. A., Ringman J., Thompson P. M., Ghetti B., Saykin A. J., Sperling R. A., Johnson K. A., Salloway S., Correia S., Schofield P. R., Masters C. L., Rowe C., Villemagne V. L., Martins R., Ourselin S., Rossor M. N., Fox N. C., Cash D. M., Weiner M. W., Holtzman D. M., Buckles V. D., Moulder K., Morris J. C., Regional variability of imaging biomarkers in autosomal dominant Alzheimer's disease, 10.1073/pnas.1317918110
  35. Altmann Andre, Ng Bernard, Landau Susan M., Jagust William J., Greicius Michael D., Regional brain hypometabolism is unrelated to regional amyloid plaque burden, 10.1093/brain/awv278
  36. Oh Hwamee, Madison Cindee, Baker Suzanne, Rabinovici Gil, Jagust William, Dynamic relationships between age, amyloid-β deposition, and glucose metabolism link to the regional vulnerability to Alzheimer’s disease, 10.1093/brain/aww108
  37. Murray Melissa E., Lowe Val J., Graff-Radford Neill R., Liesinger Amanda M., Cannon Ashley, Przybelski Scott A., Rawal Bhupendra, Parisi Joseph E., Petersen Ronald C., Kantarci Kejal, Ross Owen A., Duara Ranjan, Knopman David S., Jack Clifford R., Dickson Dennis W., Clinicopathologic and11C-Pittsburgh compound B implications of Thal amyloid phase across the Alzheimer’s disease spectrum, 10.1093/brain/awv050
  38. Thal Dietmar Rudolf, Beach Thomas G., Zanette Michelle, Heurling Kerstin, Chakrabarty Aruna, Ismail Azzam, Smith Adrian P.L., Buckley Christopher, [ 18 F]flutemetamol amyloid positron emission tomography in preclinical and symptomatic Alzheimer's disease: Specific detection of advanced phases of amyloid-β pathology, 10.1016/j.jalz.2015.05.018
  39. Wu Jessica W, Hussaini S Abid, Bastille Isle M, Rodriguez Gustavo A, Mrejeru Ana, Rilett Kelly, Sanders David W, Cook Casey, Fu Hongjun, Boonen Rick A C M, Herman Mathieu, Nahmani Eden, Emrani Sheina, Figueroa Y Helen, Diamond Marc I, Clelland Catherine L, Wray Selina, Duff Karen E, Neuronal activity enhances tau propagation and tau pathology in vivo, 10.1038/nn.4328
  40. Cohen A. D., Price J. C., Weissfeld L. A., James J., Rosario B. L., Bi W., Nebes R. D., Saxton J. A., Snitz B. E., Aizenstein H. A., Wolk D. A., DeKosky S. T., Mathis C. A., Klunk W. E., Basal Cerebral Metabolism May Modulate the Cognitive Effects of A  in Mild Cognitive Impairment: An Example of Brain Reserve, 10.1523/jneurosci.3669-09.2009
  41. Crary John F., Trojanowski John Q., Schneider Julie A., Abisambra Jose F., Abner Erin L., Alafuzoff Irina, Arnold Steven E., Attems Johannes, Beach Thomas G., Bigio Eileen H., Cairns Nigel J., Dickson Dennis W., Gearing Marla, Grinberg Lea T., Hof Patrick R., Hyman Bradley T., Jellinger Kurt, Jicha Gregory A., Kovacs Gabor G., Knopman David S., Kofler Julia, Kukull Walter A., Mackenzie Ian R., Masliah Eliezer, McKee Ann, Montine Thomas J., Murray Melissa E., Neltner Janna H., Santa-Maria Ismael, Seeley William W., Serrano-Pozo Alberto, Shelanski Michael L., Stein Thor, Takao Masaki, Thal Dietmar R., Toledo Jonathan B., Troncoso Juan C., Vonsattel Jean Paul, White Charles L., Wisniewski Thomas, Woltjer Randall L., Yamada Masahito, Nelson Peter T., Primary age-related tauopathy (PART): a common pathology associated with human aging, 10.1007/s00401-014-1349-0
  42. Duyckaerts Charles, Braak Heiko, Brion Jean-Pierre, Buée Luc, Del Tredici Kelly, Goedert Michel, Halliday Glenda, Neumann Manuela, Spillantini Maria Grazia, Tolnay Markus, Uchihara Toshiki, PART is part of Alzheimer disease, 10.1007/s00401-015-1390-7
  43. Kondo Hideki, Witter Menno P., Topographic organization of orbitofrontal projections to the parahippocampal region in rats : Orbitofrontal Projections to the Rat Parahippocampal Region, 10.1002/cne.23442
  44. Meguro K., Blaizot X., Kondoh Y., Le Mestric C., Baron J. C., Chavoix C., Neocortical and hippocampal glucose hypometabolism following neurotoxic lesions of the entorhinal and perirhinal cortices in the non-human primate as shown by PET, 10.1093/brain/122.8.1519
  45. Landau Susan M., Harvey Danielle, Madison Cindee M., Koeppe Robert A., Reiman Eric M., Foster Norman L., Weiner Michael W., Jagust William J., Associations between cognitive, functional, and FDG-PET measures of decline in AD and MCI, 10.1016/j.neurobiolaging.2009.07.002
  46. Scheef L., Spottke A., Daerr M., Joe A., Striepens N., Kolsch H., Popp J., Daamen M., Gorris D., Heneka M. T., Boecker H., Biersack H. J., Maier W., Schild H. H., Wagner M., Jessen F., Glucose metabolism, gray matter structure, and memory decline in subjective memory impairment, 10.1212/wnl.0b013e31826c1a8d
  47. Huijbers W., Vannini P., Sperling R.A., C.M. Pennartz, Cabeza R., Daselaar S.M., Explaining the encoding/retrieval flip: Memory-related deactivations and activations in the posteromedial cortex, 10.1016/j.neuropsychologia.2012.08.021
  48. Sarazin Marie, Chauviré Valérie, Gerardin Emilie, Colliot Olivier, Kinkingnéhun Serge, de Souza Leonardo Cruz, Hugonot-Diener Laurence, Garnero Line, Lehéricy Stéphane, Chupin Marie, Dubois Bruno, The Amnestic Syndrome of Hippocampal type in Alzheimer's Disease: An MRI Study, 10.3233/jad-2010-091150
  49. de Leon M. J., Convit A., Wolf O. T., Tarshish C. Y., DeSanti S., Rusinek H., Tsui W., Kandil E., Scherer A. J., Roche A., Imossi A., Thorn E., Bobinski M., Caraos C., Lesbre P., Schlyer D., Poirier J., Reisberg B., Fowler J., Prediction of cognitive decline in normal elderly subjects with 2-[18F]fluoro-2-deoxy-D-glucose/positron-emission tomography (FDG/PET), 10.1073/pnas.191044198
  50. Wheeler Mark A., Stuss Donald T., Tulving Endel, Frontal lobe damage produces episodic memory impairment, 10.1017/s1355617700000655
Bibliographic reference Hanseeuw, Bernard ; Betensky, Rebecca A. ; Schultz, Aaron P. ; Papp, Kathryn V. ; Mormino, Elizabeth C. ; et. al. Fluorodeoxyglucose metabolism associated with tau-amyloid interaction predicts memory decline : Tau, Amyloid, FDG, and Memory in Normal Aging. In: Annals of Neurology, Vol. 81, no. 4, p. 583-596 (2017)
Permanent URL http://hdl.handle.net/2078.1/190011