Bastin, Christine ✱; Université de Liège - ULiège > CRC In vivo Imaging-Aging & Memory
Bahri, Mohamed Ali ✱; Université de Liège - ULiège > CRC In vivo Imaging-Aging & Memory
Meyer, François ; Université de Liège - ULiège > CRC In vivo Imaging-Aging & Memory
Manard, Marine ; Université de Liège - ULiège > CRC In vivo Imaging-Aging & Memory
Delhaye, Emma ; Centre Hospitalier Universitaire de Liège - CHU > Département de médecine interne > Centre de jour interdisciplinaire des troubles de la mémoire
Plenevaux, Alain ; Université de Liège - ULiège > CRC In vivo Imaging-Preclinical Imaging
Becker, Guillaume ; Université de Liège - ULiège > Département de Psychologie > Département de Psychologie
Seret, Alain ; Université de Liège - ULiège > Département de physique > Imagerie médicale expérimentale
Mella, Christine ; Université de Liège - ULiège > Département des sciences cliniques > Département des sciences cliniques
Giacomelli, Fabrice
Degueldre, Christian ; Université de Liège - ULiège > CRC In vivo Imaging-Aging & Memory
Balteau, Evelyne ; Université de Liège - ULiège > CRC In vivo Im.-Neuroimaging, data acquisition & processing
Luxen, André ; Université de Liège - ULiège > Département de chimie (sciences) > Laboratoire de chimie organique de synthèse
Salmon, Eric ; Université de Liège - ULiège > Département des sciences cliniques > Neuroimagerie des troubles de la mémoire et revalid. cogn.
✱ These authors have contributed equally to this work.
Language :
English
Title :
In vivo imaging of synaptic loss in Alzheimer’s disease with [18F]UCB-H Positron Emission Tomography
Publication date :
2020
Journal title :
European Journal of Nuclear Medicine and Molecular Imaging
ISSN :
1619-7070
eISSN :
1619-7089
Publisher :
Springer, Germany
Volume :
47
Issue :
2
Pages :
390-402
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
IUAP - Interuniversity Attraction Poles Programme (IUAP 7/11); ARC - Actions de recherche concertées (ARC 12/17-01); Special Research Funds classical grant 2016 (Faculty of Medicine, University of Liege, Belgium), FRS-FNRS
Funders :
BELSPO - SPP Politique scientifique - Service Public Fédéral de Programmation Politique scientifique ULiège - Université de Liège [BE] F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, et al. Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol. 1991;30:572–80. 10.1002/ana.410300410.
Scheff SW, Price DA, Schmitt FA, Mufson EJ. Hippocampal synaptic loss in early Alzheimer’s disease and mild cognitive impairment. Neurobiol Aging. 2006;27:1372–84. 10.1016/j.neurobiolaging.2005.09.012.
Honer W. Pathology of presynaptic proteins in Alzheimer’s disease: more than simple loss of terminals. Neurobiol Aging. 2003;24:1047–62. 10.1016/j.neurobiolaging.2003.04.005.
de Wilde MC, Overk CR, Sijben JW, Masliah E. Meta-analysis of synaptic pathology in Alzheimer’s disease reveals selective molecular vesicular machinery vulnerability. Alzheimers Dement. 2016;12:633–44. 10.1016/j.jalz.2015.12.005.
Schmitz TW, Nathan Spreng R. Alzheimer’s disease neuroimaging I. Basal forebrain degeneration precedes and predicts the cortical spread of Alzheimer’s pathology. Nat Commun. 2016;7:13249. 10.1038/ncomms13249.
Counts SE, Nadeem M, Lad SP, Wuu J, Mufson EJ. Differential expression of synaptic proteins in the frontal and temporal cortex of elderly subjects with mild cognitive impairment. J Neuropathol Exp Neurol. 2006;65:592–601.
Counts SE, He B, Nadeem M, Wuu J, Scheff SW, Mufson EJ. Hippocampal drebrin loss in mild cognitive impairment. Neurodegener Dis. 2012;10:216–9. 10.1159/000333122.
Scheff SW, Price DA, Ansari MA, Roberts KN, Schmitt FA, Ikonomovic MD, et al. Synaptic change in the posterior cingulate gyrus in the progression of Alzheimer’s disease. J Alzheimers Dis. 2015;43:1073–90. 10.3233/JAD-141518.
McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, 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. 10.1016/j.jalz.2011.03.005.
Nabulsi NB, Mercier J, Holden D, Carre S, Najafzadeh S, Vandergeten MC, et al. Synthesis and preclinical evaluation of 11C-UCB-J as a PET tracer for imaging the synaptic vesicle glycoprotein 2A in the brain. J Nucl Med. 2016;57:777–84. 10.2967/jnumed.115.168179.
Estrada S, Lubberink M, Thibblin A, Sprycha M, Buchanan T, Mestdagh N, et al. [(11)C]UCB-A, a novel PET tracer for synaptic vesicle protein 2A. Nucl Med Biol. 2016;43:325–32. 10.1016/j.nucmedbio.2016.03.004.
Warnock GI, Aerts J, Bahri MA, Bretin F, Lemaire C, Giacomelli F, et al. Evaluation of 18F-UCB-H as a novel PET tracer for synaptic vesicle protein 2A in the brain. J Nucl Med. 2014;55:1336–41. 10.2967/jnumed.113.136143.
Robinson JL, Molina-Porcel L, Corrada MM, Raible K, Lee EB, Lee VM, et al. Perforant path synaptic loss correlates with cognitive impairment and Alzheimer’s disease in the oldest-old. Brain. 2014;137:2578–87. 10.1093/brain/awu190.
Chen M, Mecca AP, Naganawa M, et al. Assessing synaptic density in alzheimer disease with synaptic vesicle glycoprotein 2a positron emission tomographic imaging. JAMA Neurol. 2018. 10.1001/jamaneurol.2018.1836.
Mormino EC, Jagust WJ. A new tool for clinical neuroscience—synaptic imaging. JAMA Neurol. 2018. 10.1001/jamaneurol.2018.1643.
Becker G, Warnier C, Serrano ME, Bahri MA, Mercier J, Lemaire C, et al. Pharmacokinetic characterization of [(18)F]UCB-H PET radiopharmaceutical in the rat brain. Mol Pharm. 2017;14:2719–25. 10.1021/acs.molpharmaceut.7b00235.
Bretin F, Bahri MA, Bernard C, Warnock G, Aerts J, Mestdagh N, et al. Biodistribution and radiation dosimetry for the novel SV2A radiotracer [(18)F]UCB-H: first-in-human study. Mol Imaging Biol. 2015;17:557–64. 10.1007/s11307-014-0820-6.
Bahri MA, Plenevaux A, Aerts J, Bastin C, Becker G, Mercier J, et al. Measuring brain synaptic vesicle protein 2A with positron emission tomography and [(18)F]UCB-H. Alzheimers Dement (N Y). 2017;3:481–6. 10.1016/j.trci.2017.08.004.
Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, et al. The diagnosis of mild cognitive impairment 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;7:270–9. 10.1016/j.jalz.2011.03.008.
Jack CR Jr, Bennett DA, Blennow K, Carrillo MC, Dunn B, Haeberlein SB, et al. NIA-AA research framework: toward a biological definition of Alzheimer’s disease. Alzheimers Dement. 2018;14:535–62. 10.1016/j.jalz.2018.02.018.
Didic M, Ranjeva JP, Barbeau E, Confort-Gouny S, Fur YL, Felician O, et al. Impaired visual recognition memory in amnestic mild cognitive impairment is associated with mesiotemporal metabolic changes on magnetic resonance spectroscopic imaging. J Alzheimers Dis. 2010;22:1269–79. 10.3233/JAD-2010-101257.
Migliorelli R, Teson A, Sabe L, Petracca G, Petracchi M, Leiguarda R, et al. Anosognosia in Alzheimer’s disease: a study of associated factors. J Neuropsychiatry Clin Neurosci. 1995;7:338–44.
Clare L, Wilson BA, Carter G, Roth I, Hodges JR. Assessing awareness in early-stage Alzheimer’s disease: development and piloting of the memory awareness rating scale. Neuropsychol Rehabil. 2002;12:341–62.
Cacciamani F, Tandetnik C, Gagliardi G, Bertin H, Habert MO, Hampel H, et al. Low cognitive awareness, but not complaint, is a good marker of preclinical Alzheimer’s disease. J Alzheimers Dis. 2017;59:753–62. 10.3233/JAD-170399.
Warnier C, Lemaire C, Becker G, Zaragoza G, Giacomelli F, Aerts J, et al. Enabling efficient positron emission tomography (PET) imaging of synaptic vesicle glycoprotein 2A (SV2A) with a robust and one-step radiosynthesis of a highly potent 18F-labeled ligand ([18F]UCB-H). J Med Chem. 2016;59:8955–66. 10.1021/acs.jmedchem.6b00905.
Draganski B, Ashburner J, Hutton C, Kherif F, Frackowiak RS, Helms G, et al. Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ). Neuroimage. 2011;55:1423–34. 10.1016/j.neuroimage.2011.01.052.
Erlandsson K, Buvat I, Pretorius PH, Thomas BA, Hutton BF. A review of partial volume correction techniques for emission tomography and their applications in neurology, cardiology and oncology. Phys Med Biol. 2012;57:R119–R59. 10.1088/0031-9155/57/21/r119.
Thomas BA, Cuplov V, Bousse A, Mendes A, Thielemans K, Hutton BF, et al. PETPVC: a toolbox for performing partial volume correction techniques in positron emission tomography. Phys Med Biol. 2016;61:7975–93. 10.1088/0031-9155/61/22/7975.
Salinas CA, Searle GE, Gunn RN. The simplified reference tissue model: model assumption violations and their impact on binding potential. J Cereb Blood Flow Metab. 2015;35:304–11. 10.1038/jcbfm.2014.202.
Wahlund LO, Barkhof F, Fazekas F, Bronge L, Augustin M, Sjogren M, et al. A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke. 2001;32:1318–22.
Schain M, Benjaminsson S, Varnäs K, Forsberg A, Halldin C, Lansner A, et al. Arterial input function derived from pairwise correlations between PET-image voxels. J Cereb Blood Flow Metab. 2013;33:1058–65. 10.1038/jcbfm.2013.47.
Rousset OG, Ma Y, Evans AC. Correction for partial volume effects in PET: principle and validation. J Nucl Med. 1998;39:904–11.
Krauth A, Blanc R, Poveda A, Jeanmonod D, Morel A, Székely G. A mean three-dimensional atlas of the human thalamus: generation from multiple histological data. Neuroimage. 2010;49:2053–62. 10.1016/j.neuroimage.2009.10.042.
Zaborszky L, Hoemke L, Mohlberg H, Schleicher A, Amunts K, Zilles K. Stereotaxic probabilistic maps of the magnocellular cell groups in human basal forebrain. Neuroimage. 2008;42:1127–41. 10.1016/j.neuroimage.2008.05.055.
Garibotto V, Tettamanti M, Marcone A, Florea I, Panzacchi A, Moresco R, et al. Cholinergic activity correlates with reserve proxies in Alzheimer’s disease. Neurobiol Aging. 2013;34:2694 e13–8. 10.1016/j.neurobiolaging.2013.05.020.
Thomas BA, Erlandsson K, Modat M, Thurfjell L, Vandenberghe R, Ourselin S, et al. The importance of appropriate partial volume correction for PET quantification in Alzheimer’s disease. Eur J Nucl Med Mol Imaging. 2011;38:1104–19. 10.1007/s00259-011-1745-9.
Kepe V, Barrio JR, Huang SC, Ercoli L, Siddarth P, Shoghi-Jadid K, et al. Serotonin 1A receptors in the living brain of Alzheimer’s disease patients. Proc Natl Acad Sci U S A. 2006;103:702–7. 10.1073/pnas.0510237103.
Liu AK, Chang RC, Pearce RK, Gentleman SM. Nucleus basalis of Meynert revisited: anatomy, history and differential involvement in Alzheimer’s and Parkinson’s disease. Acta Neuropathol. 2015;129:527–40. 10.1007/s00401-015-1392-5.
Aggleton JP. Multiple anatomical systems embedded within the primate medial temporal lobe: implications for hippocampal function. Neurosci Biobehav Rev. 2012;36:1579–96. 10.1016/j.neubiorev.2011.09.005.
Johansen-Berg H, Behrens TE, Sillery E, Ciccarelli O, Thompson AJ, Smith SM, et al. Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. Cereb Cortex. 2005;15:31–9. 10.1093/cercor/bhh105.
Morris RG, Mograbi DC. Anosognosia, autobiographical memory and self knowledge in Alzheimer’s disease. Cortex. 2013;49:1553–65.
Leech R, Sharp DJ. The role of the posterior cingulate cortex in cognition and disease. Brain. 2014;137:12–32. 10.1093/brain/awt162.