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Neuroimaging of Alzheimer's Disease: Focus on Amyloid and Tau

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Neuroimaging of Alzheimer's Disease: Focus on Amyloid and Tau Japanese Journal of Radiology (2019) 37:735–749 https://doi.org/10.1007/s11604-019-00867-7 INVITED REVIEW Neuroimaging of Alzheimer’s disease: focus on amyloid and tau PET Hiroshi Matsuda1 · Yoko Shigemoto2 · Noriko Sato2 Received: 23 July 2019 / Accepted: 28 August 2019 / Published online: 6 September 2019 © Japan Radiological Society 2019 Abstract Although the diagnosis of dementia is still largely a clinical one, based on history and disease course, neuroimaging has dra- matically increased our ability to accurately diagnose it. Neuroimaging modalities now play a wider role in dementia beyond their traditional role of excluding neurosurgical lesions and are recommended in most clinical guidelines for dementia. In addition, new neuroimaging methods facilitate the diagnosis of most neurodegenerative conditions after symptom onset and show diagnostic promise even in the very early or presymptomatic phases of some diseases. In the case of Alzheimer’s disease (AD), extracellular amyloid-β (Aβ) aggregates and intracellular tau neurofbrillary tangles are the two neuropathological hallmarks of the disease. Recent molecular imaging techniques using amyloid and tau PET ligands have led to preclinical diagnosis and improved diferential diagnosis as well as narrowed subject selection and treatment monitoring in clinical trials aimed at delaying or preventing the symptomatic phase of AD. This review discusses the recent progress in amyloid and tau PET imaging and the key fndings achieved by the use of this molecular imaging modality related to the respective roles of Aβ and tau in AD, as well as its specifc limitations. Keywords Dementia · Alzheimer’s disease · PET · Amyloid · Tau Introduction expected to reach 7 million in 2025, representing approxi- mately one in fve elderly people in Japan [3]. Alzheimer’s disease (AD) is an irreversible, progressive Criteria for the clinical diagnosis of AD were established brain disorder that slowly compromises the healthy brain, by a workgroup of the National Institute of Neurological afecting memory, cognitive skills, emotions, behavior, and and Communicative Disorders and Stroke and the Alzhei- mood. Over time, a person’s ability to carry out daily activi- mer’s Disease and Related Disorders Association in 1984 ties becomes impaired. AD is the most common form of [4]. These criteria were universally adopted, have been dementia, accounting for around two-thirds of cases [1]. The extremely useful, and have survived intact without modifca- 2018 World Alzheimer Report [2] indicated that there were tion for well over a quarter of a century. However, the inter- 50 million people living with dementia worldwide, with the vening 35 years have seen advances in the understanding of number of cases projected to almost double every 20 years. AD and our ability to detect its pathophysiological process, In Japan, a 2013 study commissioned by the Ministry of as well as changes in conceptualization regarding the clini- Health, Labour, and Welfare reported that more than 4.6 cal spectrum of the disease. The pathophysiological process million Japanese were living with dementia. This number is of AD is thought to begin many years before the diagnosis of AD dementia. This long preclinical phase of AD could provide a critical opportunity for therapeutic intervention. However, we need to further elucidate the link between the * Hiroshi Matsuda pathological cascade of AD and the emergence of clinical [email protected] symptoms. The National Institute on Aging and the Alz- heimer’s Association convened an international working 1 Integrative Brain Imaging Center, National Center of Neurology and Psychiatry, 4-1-1 Ogawahigashi, Kodaira, group to review the biomarker, epidemiological, and neu- Tokyo 187-8551, Japan ropsychological evidence and to develop recommendations 2 Department of Radiology, National Center of Neurology to identify the factors that best predict the risk of progres- and Psychiatry, 4-1-1 Ogawahigashi, Kodaira, sion from normal cognition to mild cognitive impairment Tokyo 187-8551, Japan Vol.:(0123456789)1 3 736 Japanese Journal of Radiology (2019) 37:735–749 (MCI) and AD dementia [5, 6]. A conceptual framework rate of 28.8%/year, more rapidly than in the ADNI study and operational research criteria were proposed based on in the United States (20.2%). The signifcantly higher rate the prevailing scientifc evidence, as well as the testing and of conversion to dementia in the J-ADNI persisted until refnement of these models through longitudinal clinical 18 months (39.7% in the J-ADNI vs. 27.4% in the ADNI), research studies [7, 8]. whereas the rate in the ADNI caught up after 24 months, The staging of preclinical AD was also proposed [8]. reaching 45.1% in the J-ADNI and 40.9% in the ADNI at Stage 1 involves asymptomatic amyloidosis with high PET 36 months. These conversion rates are consistent with those amyloid tracer retention and low cerebrospinal fuid (CSF) described previously (7–20%) [9–13], with any variations levels of the 42-amino acid-long amyloid β (Aβ) peptide likely to be related to the diferent measures used to defne (Aβ42). Stage 2 has both amyloidosis and neurodegeneration MCI across the studies. with neuronal dysfunction on 18F-fuorodeoxy glucose (18F- Due to the recent progress in biomarkers, Jack et al. [15] FDG) PET or functional MRI, high CSF tau/phosphorylated proposed an unbiased descriptive classification scheme tau, and cortical thinning/hippocampal structure atrophy on for AD biomarkers. They proposed the “A/T/N” system in structural MRI. Stage 3 adds subtle cognitive decline to the which seven major AD biomarkers are divided into three amyloidosis and neurodegeneration with evidence of a sub- binary categories based on the nature of the pathophysiol- tle change from baseline cognition and poor performance ogy that each measures. “A” refers to the value of the Aβ on more challenging cognitive tests but does not meet the biomarker (amyloid PET or CSF Aβ42), “T”, the value of criteria for MCI. the tau biomarker (CSF phosphorylated tau or tau PET), and Patients who are memory impaired but have limited func- “N”, biomarkers of neurodegeneration or neuronal injury tional impairment and do not meet the clinical criteria for (18F-fuorodeoxyglucose PET, structural MRI, or CSF total dementia are classifed as having MCI or mild neurocogni- tau). Each biomarker category is rated as positive or nega- tive disorder as defned in the most recent Diagnostic and tive. It is agnostic to the temporal ordering of mechanisms Statistical Manual of Mental Disorders V [9–11]. MCI is underlying AD pathogenesis and is a descriptive system increasingly recognized as a major health care issue because for categorizing multidomain biomarker findings at the of its association with signifcant morbidity, including the individual level in an easy to understand and use format development of dementia and AD dementia. MCI is a het- (Table 1, Figs. 1, 2, 3, 4). Given this situation, the role of erogeneous clinical syndrome, and new criteria for MCI due amyloid and tau PET is becoming increasingly important. to AD are intended to help to increase the accuracy of AD This review presents the current state of these molecular diagnosis in the pre-dementia stage [12]. One 5-year longitu- imaging approaches in AD research. dinal epidemiological study estimated the rate at which indi- viduals with MCI progress to dementia in Nakayama, Japan [13]. Community dwellers aged 65 years and older were Amyloid PET invited to participate over a 14-month period. Overall, the annual conversion rate from MCI to dementia was reported PET ligands to be 16.1% per 100 person-years, with the conversion rate from MCI to AD dementia 8.5% per 100 person-years. In One of a number of compounds that have been developed the Japanese Alzheimer’s disease neuroimaging initiative for the imaging of amyloid, N-methyl-[11C]2-(4′-methyl- (J-ADNI) study [14], MCI patients (234 patients enrolled, aminophenyl)-6-hydroxybezothiazole or simply Pitts- 232 at baseline) progressed to dementia in 12 months at a burgh Compound-B (PiB) [16] is the derivative of the Table 1 A/T/N classifcation scheme for AD imaging biomarkes corresponding to NIA-AA classifcation A/T/N score Preclinical AD MCI probable AD dementia A−/T−/N− Not defned MCI, unlikely due to AD Dementia, unlikely due to AD A+/T−/N− Stage 1 MCI, core clinical criteria Intermediate likelihood; probable AD dementia; based on clinical criteria A+/T+/N− stage 2/3 MCI, core clinical criteria High likelihood; probable AD dementia; based on clinical criteria A+/T−/N+ Not defned MCI, core clinical criteria High likelihood; probable AD dementia; based on clinical criteria A+/T+/N+ stage 2/3 MCI due to AD, high likelihood High likelihood AD pathophysiology A−/T+/N− Not defned Not defned Probable AD dementia; based on clinical criteria A−/T−/N+ Not defned Not defned Intermediate likelihood; probable AD dementia; based on clinical criteria A−/T+/N+ Not defned Not defned Intermediate likelihood; probable AD dementia; based on clinical criteria A amyloid PET, T tau PET, N FDG-PET or MRI 1 3 Japanese Journal of Radiology (2019) 37:735–749 737 Fig. 1 Cognitively normal indi- vidual (A−/T−/N−). 11C-PiB: amyloid (A). 18F-THK5351: tau (T). MRI: neuronal injury (N). All three biomarkers are negative amyloid-binding dye thiofavin-T and the most extensively by NEPTIS, Eli Lilly, and MPS200Aβ, Sumitomo Heavy validated tracer. It binds to aggregated, fbrillar Aβ depos- Industries) and forbetaben [22] (Neuraceq, Life Molecu- its, such as those found in the cerebral cortex and striatum, lar Imaging; synthesized by Synthera, SCETI) are derived but not to amorphous Aβ deposits, such as those predomi- from stilbene. Marketing authorizations were granted by the nating in the cerebellum. The frst 11C-PiB PET study in pharmaceutical and medical devices agency for futemeta- humans [17] was performed in mild AD patients, where the mol (Vizamyl, Nihon Medi-Physics) and forbetapir (Amy- uptake pattern was consistent with the Aβ plaque deposition vid, Fuji Film Toyama Chemical), which are not reimbursed described in postmortem studies of AD brains.
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