Neuroimaging in Alzheimer's disease: preclinical challenges toward clinical efficacy

Weiner, 2015, Impact of the Alzheimer’s Disease Neuroimaging Initiative, 2004 to 2014, Alzheimers Dement J Alzheimers Assoc, 11, 865, 10.1016/j.jalz.2015.04.005 Duara, 2008, Medial temporal lobe atrophy on MRI scans and the diagnosis of Alzheimer disease, Neurology, 71, 1986, 10.1212/01.wnl.0000336925.79704.9f Ferreira, 2015, Brain changes in Alzheimer's disease patients with implanted encapsulated cells releasing nerve growth factor, J Alzheimers Dis, 43, 1059, 10.3233/JAD-141068 Hsu, 2015, Amyloid burden in cognitively normal elderly is associated with preferential hippocampal subfield volume loss, J Alzheimers Dis JAD, 45, 27, 10.3233/JAD-141743 Trzepacz, 2015, Relationship of hippocampal volume to amyloid burden across diagnostic stages of Alzheimer's disease, Dement Geriatr Cogn Disord, 41, 68, 10.1159/000441351 Yin, 2014, Association of amyloid burden, brain atrophy and memory deficits in aged apolipoprotein ε4 mice, Curr Alzheimer Res, 11, 283, 10.2174/156720501103140329220007 Bernard, 2014, Time course of brain volume changes in the preclinical phase of Alzheimer's disease, Alzheimers Dement J Alzheimers Assoc, 10, 143, 10.1016/j.jalz.2013.08.279 Firbank, 2016, Longitudinal diffusion tensor imaging in dementia with Lewy bodies and Alzheimer's disease, Parkinsonism Relat Disord, 24, 76, 10.1016/j.parkreldis.2016.01.003 Daianu, 2015, An advanced white matter tract analysis in frontotemporal dementia and early-onset Alzheimer's disease, Brain Imaging Behav Hořínek, 2015, Difference in white matter microstructure in differential diagnosis of normal pressure hydrocephalus and Alzheimer's disease, Clin Neurol Neurosurg, 140, 52, 10.1016/j.clineuro.2015.11.010 Delli Pizzi, 2015, Structural connectivity is differently altered in dementia with Lewy body and Alzheimer's disease, Front Aging Neurosci, 7, 208, 10.3389/fnagi.2015.00208 Pautler, 2004, Mouse MRI: concepts and applications in physiology, Physiol Bethesda Md, 19, 168, 10.1152/physiol.00016.2004 Liu, 2015, Impaired parahippocampus connectivity in mild cognitive impairment and Alzheimer's disease, J Alzheimers Dis JAD, 49, 1051, 10.3233/JAD-150727 Hafkemeijer, 2015, Resting state functional connectivity differences between behavioral variant frontotemporal dementia and Alzheimer's disease, Front Hum Neurosci, 9, 474, 10.3389/fnhum.2015.00474 Zippo, 2015, The compression flow as a measure to estimate the brain connectivity changes in resting state fMRI and 18FDG-PET Alzheimer's disease connectomes, Front Comput Neurosci, 9, 148, 10.3389/fncom.2015.00148 Hanaoka, 2015, Relationship between white matter lesions and regional cerebral blood flow changes during longitudinal follow up in Alzheimer's disease, Geriatr Gerontol Int Wierenga, 2014, Cerebral blood flow measured by arterial spin labeling MRI as a preclinical marker of Alzheimer's disease, J Alzheimers Dis JAD, 42, S411, 10.3233/JAD-141467 Klunk, 2002, Imaging Abeta plaques in living transgenic mice with multiphoton microscopy and methoxy-X04, a systemically administered Congo red derivative, J Neuropathol Exp Neurol, 61, 797, 10.1093/jnen/61.9.797 Klunk, 2003, Imaging the pathology of Alzheimer's disease: amyloid-imaging with positron emission tomography, Neuroimaging Clin N Am, 13, 781, 10.1016/S1052-5149(03)00092-3 Clark, 2012, Cerebral PET with florbetapir compared with neuropathology at autopsy for detection of neuritic amyloid-β plaques: a prospective cohort study, Lancet Neurol, 11, 669, 10.1016/S1474-4422(12)70142-4 Chien, 2013, Early clinical PET imaging results with the novel PHF-tau radioligand [F-18]-T807, J Alzheimers Dis JAD, 34, 457, 10.3233/JAD-122059 Chien, 2014, Early clinical PET imaging results with the novel PHF-tau radioligand [F18]-T808, J Alzheimers Dis JAD, 38, 171, 10.3233/JAD-130098 Small, 2015, Current and future treatments for Alzheimer disease, Am J Geriatr Psychiatry, 23, 1101, 10.1016/j.jagp.2015.08.006 Benveniste, 1999, Detection of neuritic plaques in Alzheimer's disease by magnetic resonance microscopy, Proc Natl Acad Sci U S A, 96, 14079, 10.1073/pnas.96.24.14079 Dhenain, 2002, Senile plaques do not induce susceptibility effects in T2*-weighted MR microscopic images, NMR Biomed, 15, 197, 10.1002/nbm.760 Dhenain, 2006, Passive staining: a novel ex vivo MRI protocol to detect amyloid deposits in mouse models of Alzheimer's disease, Magn Reson Med, 55, 687, 10.1002/mrm.20810 Chamberlain, 2009, Comparison of amyloid plaque contrast generated by T2-weighted, T2*-weighted, and susceptibility-weighted imaging methods in transgenic mouse models of Alzheimer's disease, Magn Reson Med, 61, 1158, 10.1002/mrm.21951 Pérez-Torres, 2014, Use of magnetization transfer contrast MRI to detect early molecular pathology in Alzheimer's disease, Magn Reson Med, 71, 333, 10.1002/mrm.24665 Bigot, 2014, Magnetization transfer contrast imaging reveals amyloid pathology in Alzheimer's disease transgenic mice, Neuroimage, 87, 111, 10.1016/j.neuroimage.2013.10.056 Park, 2009, Paramagnetic ultrasmall gadolinium oxide nanoparticles as advanced T1 MRI contrast agent: account for large longitudinal relaxivity, optimal particle diameter, and in vivo T1 MR images, ACS Nano, 3, 3663, 10.1021/nn900761s Faucher, 2011, Impact of agglomeration on the relaxometric properties of paramagnetic ultra-small gadolinium oxide nanoparticles, Nanotechnology, 22, 295103, 10.1088/0957-4484/22/29/295103 Stankiewicz, 2007, Iron in chronic brain disorders: imaging and neurotherapeutic implications, Neurother J Am Soc Exp Neurother, 4, 371, 10.1016/j.nurt.2007.05.006 Sperling, 2011, Amyloid related imaging abnormalities (ARIA) in amyloid modifying therapeutic trials: recommendations from the Alzheimer's Association Research Roundtable Workgroup, Alzheimers Dement J Alzheimers Assoc, 7, 367, 10.1016/j.jalz.2011.05.2351 Leike, 2001, Characterization of continuously extruded iopromide-carrying liposomes for computed tomography blood-pool imaging, Invest Radiol, 36, 303, 10.1097/00004424-200106000-00001 Sachse, 1997, Biodistribution and computed tomography blood-pool imaging properties of polyethylene glycol-coated iopromide-carrying liposomes, Invest Radiol, 32, 44, 10.1097/00004424-199701000-00007 Sachse, 1993, Preparation and evaluation of lyophilized iopromide-carrying liposomes for liver tumor detection, Invest Radiol, 28, 838, 10.1097/00004424-199328090-00019 Burke, 2007, Imaging of pulmonary embolism and t-PA therapy effects using MDCT and liposomal iohexol blood pool agent: preliminary results in a rabbit model, Acad Radiol, 14, 355, 10.1016/j.acra.2006.12.014 Karathanasis, 2009, Imaging nanoprobe for prediction of outcome of nanoparticle chemotherapy by using mammography, Radiology, 250, 398, 10.1148/radiol.2502080801 Karathanasis, 2008, Multifunctional nanocarriers for mammographic quantification of tumor dosing and prognosis of breast cancer therapy, Biomaterials, 29, 4815, 10.1016/j.biomaterials.2008.08.036 Ghaghada, 2011, Evaluation of tumor microenvironment in an animal model using a nanoparticle contrast agent in computed tomography imaging, Acad Radiol, 18, 20, 10.1016/j.acra.2010.09.003 Ashton, 2014, Dual-energy micro-CT functional imaging of primary lung cancer in mice using gold and iodine nanoparticle contrast agents: a validation study, PLoS One, 9, e88129, 10.1371/journal.pone.0088129 Bell, 2012, Data analysis: evaluation of nanoscale contrast agent enhanced CT scan to differentiate between benign and malignant lung cancer in mouse model, AMIA Annu Symp Proc, 2012, 27 Bhavane, 2013, Dual-energy computed tomography imaging of atherosclerotic plaques in a mouse model using a liposomal-iodine nanoparticle contrast agent, Circ Cardiovasc Imaging, 6, 285, 10.1161/CIRCIMAGING.112.000119 Starosolski, 2015, Ultra high-resolution in vivo computed tomography imaging of mouse cerebrovasculature using a long circulating blood pool contrast agent, Sci Rep, 5, 10178, 10.1038/srep10178 Tanifum, 2014, Cerebral vascular leak in a mouse model of amyloid neuropathology, J Cereb Blood Flow Metab, 34, 1646, 10.1038/jcbfm.2014.125 Barsky, 1992, Theory of paramagnetic contrast agents in liposome systems, Magn Reson Med, 24, 1, 10.1002/mrm.1910240102 Mulder, 2006, Lipid-based nanoparticles for contrast-enhanced MRI and molecular imaging, NMR Biomed, 19, 142, 10.1002/nbm.1011 Gløgård, 2002, Liposomes as carriers of amphiphilic gadolinium chelates: the effect of membrane composition on incorporation efficacy and in vitro relaxivity, Int J Pharm, 233, 131, 10.1016/S0378-5173(01)00935-8 Ghaghada, 2009, New dual mode gadolinium nanoparticle contrast agent for magnetic resonance imaging, PLoS One, 4, e7628, 10.1371/journal.pone.0007628 Howles, 2009, High-resolution magnetic resonance angiography in the mouse using a nanoparticle blood-pool contrast agent, Magn Reson Med, 62, 1447, 10.1002/mrm.22154 Ayyagari, 2006, Long-circulating liposomal contrast agents for magnetic resonance imaging, Magn Reson Med, 55, 1023, 10.1002/mrm.20846 Ghaghada, 2007, High-resolution vascular imaging of the rat spine using liposomal blood pool MR agent, AJNR Am J Neuroradiol, 28, 48 Bucholz, 2008, Four-dimensional MR microscopy of the mouse heart using radial acquisition and liposomal gadolinium contrast agent, Magn Reson Med, 60, 111, 10.1002/mrm.21618 Bucholz, 2010, Cardiovascular phenotyping of the mouse heart using a 4D radial acquisition and liposomal Gd-DTPA-BMA, Magn Reson Med, 63, 979, 10.1002/mrm.22259 Karathanasis, 2008, MRI mediated, non-invasive tracking of intratumoral distribution of nanocarriers in rat glioma, Nanotechnology, 19, 315101, 10.1088/0957-4484/19/31/315101 Aime, 2009, Pushing the sensitivity envelope of lanthanide-based magnetic resonance imaging (MRI) contrast agents for molecular imaging applications, Acc Chem Res, 42, 822, 10.1021/ar800192p Aime, 2007, Gd-loaded liposomes as T1, susceptibility, and CEST agents, all in one, J Am Chem Soc, 129, 2430, 10.1021/ja0677867 Opina, 2011, TmDOTA-tetraglycinate encapsulated liposomes as pH-sensitive LipoCEST agents, PLoS One, 6, e27370, 10.1371/journal.pone.0027370 Haris, 2013, MICEST: a potential tool for non-invasive detection of molecular changes in Alzheimer's disease, J Neurosci Methods, 212, 87, 10.1016/j.jneumeth.2012.09.025 Lee, 1995, Folate-mediated tumor cell targeting of liposome-entrapped doxorubicin in vitro, Biochim Biophys Acta, 1233, 134, 10.1016/0005-2736(94)00235-H Caravan, 1999, Gadolinium(III) chelates as MRI contrast agents: structure, dynamics, and applications, Chem Rev, 99, 2293, 10.1021/cr980440x Caravan, 2009, Influence of molecular parameters and increasing magnetic field strength on relaxivity of gadolinium- and manganese-based T1 contrast agents, Contrast Media Mol Imaging, 4, 89, 10.1002/cmmi.267 Bertini, 2004, Persistent contrast enhancement by sterically stabilized paramagnetic liposomes in murine melanoma, Magn Reson Med, 52, 669, 10.1002/mrm.20189 Jaruszewski, 2014, Multimodal nanoprobes to target cerebrovascular amyloid in Alzheimer's disease brain, Biomaterials, 35, 1967, 10.1016/j.biomaterials.2013.10.075 Jacoby, 2014, Probing different perfluorocarbons for in vivo inflammation imaging by 19F MRI: image reconstruction, biological half-lives and sensitivity, NMR Biomed, 27, 261, 10.1002/nbm.3059 Balducci, 2012, Visualizing arthritic inflammation and therapeutic response by fluorine-19 magnetic resonance imaging (19F MRI), J Inflamm Lond Engl, 9, 24, 10.1186/1476-9255-9-24 Temme, 2012, 19F magnetic resonance imaging of endogenous macrophages in inflammation, Wiley Interdiscip Rev Nanomed Nanobiotechnol, 4, 329, 10.1002/wnan.1163 Weise, 2011, In vivo imaging of stepwise vessel occlusion in cerebral photothrombosis of mice by 19F MRI, PLoS One, 6, e28143, 10.1371/journal.pone.0028143 Hertlein, 2011, Visualization of abscess formation in a murine thigh infection model of Staphylococcus aureus by 19F-magnetic resonance imaging (MRI), PLoS One, 6, e18246, 10.1371/journal.pone.0018246 Ebner, 2010, Early assessment of pulmonary inflammation by 19F MRI in vivo, Circ Cardiovasc Imaging, 3, 202, 10.1161/CIRCIMAGING.109.902312 Kim, 2003, Interplay of tumor vascular oxygenation and tumor pO2 observed using near-infrared spectroscopy, an oxygen needle electrode, and 19F MR pO2 mapping, J Biomed Opt, 8, 53, 10.1117/1.1527049 Hitchens, 2011, 19F MRI detection of acute allograft rejection with in vivo perfluorocarbon labeling of immune cells, Magn Reson Med, 65, 1144, 10.1002/mrm.22702 Ahrens, 2014, Clinical cell therapy imaging using a perfluorocarbon tracer and fluorine-19 MRI, Magn Reson Med, 72, 1696, 10.1002/mrm.25454 Higuchi, 2005, 19F and 1H MRI detection of amyloid beta plaques in vivo, Nat Neurosci, 8, 527, 10.1038/nn1422 Flaherty, 2007, Polyfluorinated bis-styrylbenzene beta-amyloid plaque binding ligands, J Med Chem, 50, 4986, 10.1021/jm070085f Yanagisawa, 2014, Preferred features of a fluorine-19 MRI probe for amyloid detection in the brain, J Alzheimers Dis JAD, 39, 617, 10.3233/JAD-131025 Tooyama, 2016, Amyloid imaging using fluorine-19 magnetic resonance imaging ((19)F-MRI), Ageing Res Rev, 10.1016/j.arr.2015.12.008 Pautler, 2004, In vivo, trans-synaptic tract-tracing utilizing manganese-enhanced magnetic resonance imaging (MEMRI), NMR Biomed, 17, 595, 10.1002/nbm.942 Massaad, 2011, Manganese-enhanced magnetic resonance imaging (MEMRI), Methods Mol Biol Clifton NJ, 711, 145, 10.1007/978-1-61737-992-5_7 Smith, 2011, R-flurbiprofen improves axonal transport in the Tg2576 mouse model of Alzheimer's disease as determined by MEMRI, Magn Reson Med, 65, 1423, 10.1002/mrm.22733 Serrano, 2008, Assessing transneuronal dysfunction utilizing manganese-enhanced MRI (MEMRI), Magn Reson Med, 60, 169, 10.1002/mrm.21648 Pautler, 2003, In vivo trans-synaptic tract tracing from the murine striatum and amygdala utilizing manganese enhanced MRI (MEMRI), Magn Reson Med, 50, 33, 10.1002/mrm.10498 Inoue, 2011, Manganese enhanced MRI (MEMRI): neurophysiological applications, Rev Neurosci, 22, 675, 10.1515/RNS.2011.048 Pautler, 1998, In vivo neuronal tract tracing using manganese-enhanced magnetic resonance imaging, Magn Reson Med, 40, 740, 10.1002/mrm.1910400515 Murray, 1999, Neuronal regeneration: lessons from the olfactory system, Semin Cell Dev Biol, 10, 421, 10.1006/scdb.1999.0329 Pautler, 2006, Biological applications of manganese-enhanced magnetic resonance imaging, Methods Mol Med, 124, 365 Sharma, 2010, Hyperglycemia induces oxidative stress and impairs axonal transport rates in mice, PLoS One, 5, e13463, 10.1371/journal.pone.0013463 Smith, 2007, In vivo axonal transport rates decrease in a mouse model of Alzheimer's disease, Neuroimage, 35, 1401, 10.1016/j.neuroimage.2007.01.046 Smith, 2010, Increased human wild type tau attenuates axonal transport deficits caused by loss of APP in mouse models, Magn Reson Insights, 4, 11 Hu, 2001, Manganese-enhanced MRI of mouse heart during changes in inotropy, Magn Reson Med, 46, 884, 10.1002/mrm.1273 Pautler, 2002, Tracing odor-induced activation in the olfactory bulbs of mice using manganese-enhanced magnetic resonance imaging, Neuroimage, 16, 441, 10.1006/nimg.2002.1075 Saar, 2015, Laminar specific detection of APP induced neurodegeneration and recovery using MEMRI in an olfactory based Alzheimer's disease mouse model, Neuroimage, 118, 183, 10.1016/j.neuroimage.2015.05.045 Gallagher, 2012, Deficits in axonal transport in hippocampal-based circuitry and the visual pathway in APP knock-out animals witnessed by manganese enhanced MRI, Neuroimage, 60, 1856, 10.1016/j.neuroimage.2012.01.132 Kim, 2011, Quantitative in vivo measurement of early axonal transport deficits in a triple transgenic mouse model of Alzheimer's disease using manganese-enhanced MRI, Neuroimage, 56, 1286, 10.1016/j.neuroimage.2011.02.039 Massaad, 2010, Mitochondrial superoxide contributes to blood flow and axonal transport deficits in the Tg2576 mouse model of Alzheimer's disease, PLoS One, 5, e10561, 10.1371/journal.pone.0010561 Majid, 2014, In vivo axonal transport deficits in a mouse model of fronto-temporal dementia, Neuroimage Clin, 4, 711, 10.1016/j.nicl.2014.02.005 Massaad, 2009, Overexpression of SOD-2 reduces hippocampal superoxide and prevents memory deficits in a mouse model of Alzheimer's disease, Proc Natl Acad Sci U S A, 106, 13576, 10.1073/pnas.0902714106 Pipe, 2006, Turboprop: improved PROPELLER imaging, Magn Reson Med, 55, 380, 10.1002/mrm.20768 Bhavsar, 2014, Fast, variable system delay correction for spiral MRI, Magn Reson Med, 71, 773, 10.1002/mrm.24730 Li, 2011, X-PROP: a fast and robust diffusion-weighted propeller technique, Magn Reson Med, 66, 341, 10.1002/mrm.23033 Barthel, 2015, PET/MR in dementia and other neurodegenerative diseases, Semin Nucl Med, 45, 224, 10.1053/j.semnuclmed.2014.12.003