Evaluation of [18F]PI-2620, a second-generation selective tau tracer, for assessing four-repeat tauopathies

Brain Communications - Tập 3 Số 4 - 2021
Toshiki Tezuka1, Keisuke Takahata2,3, Morinobu Seki1, Hajime Tabuchi3, Yuki Momota3, Mika Shiraiwa3, Natsumi Suzuki3, Ayaka Morimoto3, Tadaki Nakahara4, Yu Iwabuchi4, Eisuke Miura5, Yasuharu Yamamoto3, Yasunori Sano3, Kei Funaki3, Bun Yamagata3, Ryo Ueda6, Takahito Yoshizaki1, Kyoko Mashima7, Mamoru Shibata1,8, Munenori Oyama1, Kensuke Okada1, Masahito Kubota1, Hajime Okita5, Masaki Takao9,10, Masahiro Jinzaki4, Jin Nakahara1, Masaru Mimura3, Daisuke Ito1
1Department of Neurology, Keio University School of Medicine, Tokyo, Japan
2Department of Functional Brain Imaging Research, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba, Japan
3Department of Neuropsychiatry, Keio University School of Medicine, Tokyo, Japan
4Department of Diagnostic Radiology, Keio University School of Medicine, Tokyo 160-8582, Japan
5Department of Pathology, Keio University School of Medicine, Tokyo 160-8582, Japan
6Office of Radiation Technology, Keio University Hospital, Tokyo 160-8582, Japan
7Department of Neurology, Tokyo Saiseikai Central Hospital, Tokyo 108-0073, Japan
8Department of Neurology, Tokyo Dental College Ichikawa General Hospital, Tokyo 272-8513, Japan
9Brain Bank, Mihara Memorial Hospital, Gunma 372-0006, Japan
10Department of Clinical Laboratory, National Center of Neurology and Psychiatry (NCNP), National Center Hospital, Tokyo 187-8551, Japan

Tóm tắt

Abstract Tau aggregates represent a key pathologic feature of Alzheimer’s disease and other neurodegenerative diseases. Recently, PET probes have been developed for in vivo detection of tau accumulation; however, they are limited because of off-target binding and a reduced ability to detect tau in non-Alzheimer’s disease tauopathies. The novel tau PET tracer, [18F]PI-2620, has a high binding affinity and specificity for aggregated tau; therefore, it was hypothesized to have desirable properties for the visualization of tau accumulation in Alzheimer’s disease and non-Alzheimer’s disease tauopathies. To assess the ability of [18F]PI-2620 to detect regional tau burden in non-Alzheimer’s disease tauopathies compared with Alzheimer’s disease, patients with progressive supranuclear palsy (n = 3), corticobasal syndrome (n = 2), corticobasal degeneration (n = 1) or Alzheimer’s disease (n = 8), and healthy controls (n = 7) were recruited. All participants underwent MRI, amyloid β assessment and [18F]PI-2620 PET (Image acquisition at 60–90 min post-injection). Cortical and subcortical tau accumulations were assessed by calculating standardized uptake value ratios using [18F]PI-2620 PET. For pathologic validation, tau pathology was assessed using tau immunohistochemistry and compared with [18F]PI-2620 retention in an autopsied case of corticobasal degeneration. In Alzheimer’s disease, focal retention of [18F]PI-2620 was evident in the temporal and parietal lobes, precuneus, and cingulate cortex. Standardized uptake value ratio analyses revealed that patients with non-Alzheimer’s disease tauopathies had elevated [18F]PI-2620 uptake only in the globus pallidus, as compared to patients with Alzheimer’s disease, but not healthy controls. A head-to-head comparison of [18F]PI-2620 and [18F]PM-PBB3, another tau PET probe for possibly visualizing the four-repeat tau pathogenesis in non-Alzheimer’s disease, revealed different retention patterns in one subject with progressive supranuclear palsy. Imaging-pathology correlation analysis of the autopsied patient with corticobasal degeneration revealed no significant correlation between [18F]PI-2620 retention in vivo. High [18F]PI-2620 uptake at 60–90 min post-injection in the globus pallidus may be a sign of neurodegeneration in four-repeat tauopathy, but not necessarily practical for diagnosis of non-Alzheimer’s disease tauopathies. Collectively, this tracer is a promising tool to detect Alzheimer’s disease-tau aggregation. However, late acquisition PET images of [18F]PI-2620 may have limited utility for reliable detection of four-repeat tauopathy because of lack of correlation between post-mortem tau pathology and different retention pattern than the non-Alzheimer’s disease-detectable tau radiotracer, [18F]PM-PBB3. A recent study reported that [18F]PI-2620 tracer kinetics curves in four-repeat tauopathies peak earlier (within 30 min) than Alzheimer’s disease; therefore, further studies are needed to determine appropriate PET acquisition times that depend on the respective interest regions and diseases.

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Tài liệu tham khảo

Klunk, 2004, Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B, Ann Neurol, 55, 306, 10.1002/ana.20009

Maruyama, 2013, Imaging of tau pathology in a tauopathy mouse model and in Alzheimer patients compared to normal controls, Neuron, 79, 1094, 10.1016/j.neuron.2013.07.037

Lohith, 2019, Brain imaging of Alzheimer dementia patients and elderly controls with (18)F-MK-6240, a PET tracer targeting neurofibrillary tangles, J Nucl Med, 60, 107, 10.2967/jnumed.118.208215

Tagai, 2021, High-contrast in vivo imaging of tau pathologies in Alzheimer's and non-Alzheimer's disease tauopathies, Neuron, 109, 42, 10.1016/j.neuron.2020.09.042

Takahata, 2019, PET-detectable tau pathology correlates with long-term neuropsychiatric outcomes in patients with traumatic brain injury, Brain, 142, 3265, 10.1093/brain/awz238

Endo, 2019, In vivo binding of a tau imaging probe, [(11) C]PBB3, in patients with progressive supranuclear palsy, Mov Disord, 34, 744, 10.1002/mds.27643

Schonhaut, 2017, (18) F-flortaucipir tau positron emission tomography distinguishes established progressive supranuclear palsy from controls and Parkinson disease: A multicenter study, Ann Neurol, 82, 622, 10.1002/ana.25060

Smith, 2017, In vivo retention of (18)F-AV-1451 in corticobasal syndrome, Neurology, 89, 845, 10.1212/WNL.0000000000004264

Passamonti, 2017, 18F-AV-1451 positron emission tomography in Alzheimer's disease and progressive supranuclear palsy, Brain, 140, 781

Marquie, 2017, Pathological correlations of [F-18]-AV-1451 imaging in non-alzheimer tauopathies, Ann Neurol, 81, 117, 10.1002/ana.24844

Kroth, 2019, Discovery and preclinical characterization of [(18)F]PI-2620, a next-generation tau PET tracer for the assessment of tau pathology in Alzheimer's disease and other tauopathies, Eur J Nucl Med Mol Imaging, 46, 2178, 10.1007/s00259-019-04397-2

Rosler, 2019, Four-repeat tauopathies, Prog Neurobiol, 180, 101644, 10.1016/j.pneurobio.2019.101644

Mormino, 2020, Tau PET imaging with (18)F-PI-2620 in aging and neurodegenerative diseases, Eur J Nucl Med Mol Imaging, 48, 2233, 10.1007/s00259-020-04923-7

Brendel, 2020, Assessment of 18F-PI-2620 as a biomarker in progressive supranuclear palsy, JAMA Neurol, 77, 1408, 10.1001/jamaneurol.2020.2526

Soleimani-Meigooni, 2020, 18F-flortaucipir PET to autopsy comparisons in Alzheimer's disease and other neurodegenerative diseases, Brain, 143, 3477, 10.1093/brain/awaa276

Ghirelli, 2020, Sensitivity-specificity of tau and amyloid beta positron emission tomography in frontotemporal lobar degeneration, Ann Neurol, 88, 1009, 10.1002/ana.25893

Lowe, 2020, Tau-positron emission tomography correlates with neuropathology findings, Alzheimers Dement, 16, 561, 10.1016/j.jalz.2019.09.079

Ishizuchi, 2021, A case of progressive supranuclear palsy with predominant cerebellar ataxia diagnosed by [(18)F]PM-PBB3 tau PET, J Neurol Sci, 425, 117440, 10.1016/j.jns.2021.117440

Mashima, 2021, A case of tauopathy with auditory agnosia and dysprosody diagnosed by [(18)F]PM-PBB3 tau PET scan, Neurol Sci, 42, 3471, 10.1007/s10072-021-05287-y

McKhann, 2011, 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, 263, 10.1016/j.jalz.2011.03.005

Hoglinger, 2017, Clinical diagnosis of progressive supranuclear palsy: The movement disorder society criteria, Mov Disord, 32, 853, 10.1002/mds.26987

Armstrong, 2013, Criteria for the diagnosis of corticobasal degeneration, Neurology, 80, 496, 10.1212/WNL.0b013e31827f0fd1

Rosen, 1984, A new rating scale for Alzheimer's disease, Am J Psychiatry, 141, 1356, 10.1176/ajp.141.11.1356

Crowe, 1998, The differential contribution of mental tracking, cognitive flexibility, visual search, and motor speed to performance on parts A and B of the Trail Making Test, J Clin Psychol, 54, 585, 10.1002/(SICI)1097-4679(199808)54:5<585::AID-JCLP4>3.0.CO;2-K

Goetz, 2008, Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results, Mov Disord, 23, 2129, 10.1002/mds.22340

Golbe, 2007, A clinical rating scale for progressive supranuclear palsy, Brain, 130, 1552, 10.1093/brain/awm032

Iglesias, 2015, Bayesian segmentation of brainstem structures in MRI, Neuroimage, 113, 184, 10.1016/j.neuroimage.2015.02.065

Lowe, 1997, Greenfield’s neuropathology, 6th ed

Jellinger, 1971, Progressive supranuclear palsy (subcortical argyrophilic dystrophy), Acta Neuropathol, 19, 347, 10.1007/BF00692156

Arai, 1999, Mossy fiber involvement in progressive supranuclear palsy, Acta Neuropathol, 98, 341, 10.1007/s004010051091

Dickson, 1999, Neuropathologic differentiation of progressive supranuclear palsy and corticobasal degeneration, J Neurol, 246 (Suppl 2, II6, 10.1007/BF03161076

Forman, 2002, Signature tau neuropathology in gray and white matter of corticobasal degeneration, Am J Pathol, 160, 2045, 10.1016/S0002-9440(10)61154-6

Kovacs, 2020, Distribution patterns of tau pathology in progressive supranuclear palsy, Acta Neuropathol, 140, 99, 10.1007/s00401-020-02158-2

Mashima, 2017, Extremely low prevalence of amyloid positron emission tomography positivity in Parkinson's disease without dementia, Eur Neurol, 77, 231, 10.1159/000464322

Seibyl, 2016, Impact of training method on the robustness of the visual assessment of 18F-Florbetaben PET scans: Results from a phase-3 study, J Nucl Med, 57, 900, 10.2967/jnumed.115.161927

Dickson, 2002, Office of Rare Diseases neuropathologic criteria for corticobasal degeneration, J Neuropathol Exp Neurol, 61, 935, 10.1093/jnen/61.11.935

Lowe, 2016, An autoradiographic evaluation of AV-1451 Tau PET in dementia, Acta Neuropathol Commun, 4, 58, 10.1186/s40478-016-0315-6

Ono, 2017, Distinct binding of PET ligands PBB3 and AV-1451 to tau fibril strains in neurodegenerative tauopathies, Brain, 140, 764

Palleis, 2021, Cortical [(18) F]PI-2620 binding differentiates corticobasal syndrome subtypes, Mov Disord, 10.1002/mds.28624

Kikuchi, 2016, In vivo visualization of tau deposits in corticobasal syndrome by 18F-THK5351 PET, Neurology, 87, 2309, 10.1212/WNL.0000000000003375

Brendel, 2017, [(18)F]-THK5351 PET correlates with topology and symptom severity in progressive supranuclear palsy, Front Aging Neurosci, 9, 440, 10.3389/fnagi.2017.00440

Leuzy, 2020, Diagnostic performance of RO948 F 18 tau positron emission tomography in the differentiation of Alzheimer disease from other neurodegenerative disorders, JAMA Neurol, 77, 955, 10.1001/jamaneurol.2020.0989

Ishiki, 2017, Tau imaging with [(18) F]THK-5351 in progressive supranuclear palsy, Eur J Neurol, 24, 130, 10.1111/ene.13164

Arima, 2006, Ultrastructural characteristics of tau filaments in tauopathies: Immuno-electron microscopic demonstration of tau filaments in tauopathies, Neuropathology, 26, 475, 10.1111/j.1440-1789.2006.00669.x

Arai, 2004, Identification of amino-terminally cleaved tau fragments that distinguish progressive supranuclear palsy from corticobasal degeneration, Ann Neurol, 55, 72, 10.1002/ana.10793

Mueller, 2020, Tau PET imaging with (18)F-PI-2620 in patients with Alzheimer disease and healthy controls: A first-in-humans study, J Nucl Med, 61, 911, 10.2967/jnumed.119.236224

Marquie, 2017, Lessons learned about [F-18]-AV-1451 off-target binding from an autopsy-confirmed Parkinson's case, Acta Neuropathol Commun, 5, 75, 10.1186/s40478-017-0482-0

Choi, 2018, Off-target (18)F-AV-1451 binding in the basal ganglia correlates with age-related iron accumulation, J Nucl Med, 59, 117, 10.2967/jnumed.117.195248

Marquie, 2015, Validating novel tau positron emission tomography tracer [F-18]-AV-1451 (T807) on postmortem brain tissue, Ann Neurol, 78, 787, 10.1002/ana.24517

Aiba, 2012, [Corticobasal syndrome: Recent advances and future directions], Brain Nerve, 64, 462

Schneider, 1997, Corticobasal degeneration: Neuropathologic and clinical heterogeneity, Neurology, 48, 959, 10.1212/WNL.48.4.959

Chiotis, 2016, Imaging in-vivo tau pathology in Alzheimer's disease with THK5317 PET in a multimodal paradigm, Eur J Nucl Med Mol Imaging, 43, 1686, 10.1007/s00259-016-3363-z

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Tập 3 Số 4

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