Current Trends and Applications of PET/MRI Hybrid Imaging in Neurodegenerative Diseases and Normal Aging
Abstract
:1. Introduction
2. Methods
3. Results
4. Discussion
4.1. Artificial Intelligence
4.2. Technical Improvements
4.2.1. Attenuation Correction
4.2.2. Motion Correction
4.2.3. Tracer and Imaging Techniques
4.3. Functional Connectivity
4.4. Brain Regions of Interest and Biomarkers
4.4.1. Hippocampus
4.4.2. Gray and White Matter
4.4.3. Biomarker Evaluation
4.5. Associated Illnesses
4.6. Scanners
4.7. Comparison to MRI or PET
4.8. Limitations
4.9. Ongoing Challenges and Future Directions of Hybrid Imaging
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
MRI | Magnetic Resonance Imaging |
MRI-ASL | MRI-Arterial Spin Labeling |
FDG-PET | Fluorodeoxyglucose Positron-Emission Tomography |
FTD | Frontotemporal Dementia |
HC | Healthy Control |
Aß | Amyloid Beta |
PD | Parkinson’s Disease |
DLB | Dementia with Lewy Bodies |
CSF | Cerebrospinal Fluid |
P-tau181 | Phosphorylated Tau at position 181 |
AD | Alzheimer’s Disease |
MCI | Mild Cognitive Impairment |
TOF-MRI | Time-of-Flight MRI |
DTI | Diffusion Tensor Imaging |
LBD | Lewy Body Dementia |
CI | Cognitive Impairment |
eAD | Early Alzheimer’s Disease |
bvFTD | Behavioral variant Frontotemporal Dementia |
preAD | Pre-Alzheimer’s Disease |
DKI | Diffusional Kurtosis Imaging |
AWF | Axonal Water Fraction |
CBD | Corticobasal Degeneration |
FTLD/PPA | Frontotemporal Lobar Degeneration/Primary Progressive Aphasia |
FC | Functional Connectivity |
PCA | Posterior Cortical Atrophy |
SD | Semantic Dementia |
aMCI | Amnestic Mild Cognitive Impairment |
SCD | Subjective Cognitive Decline |
BOLD-FC | Blood Oxygen Level-Dependent Functional Connectivity |
MMSE | Mini-Mental State Examination |
NPH | Normal Pressure Hydrocephalus |
RS-fMRI | Resting-State Functional MRI |
SUVR | Standardized Uptake Value Ratio |
EOFAD | Early Onset Familial Alzheimer’s Disease |
PD-MCI | Parkinson’s Disease with Mild Cognitive Impairment |
FCSRT | Free and Cued Selective Reminding Test |
R-MEG | Resting-State Magnetoencephalography |
FAD | Familial Alzheimer’s Disease |
WMHV | White Matter Hyperintensity Volume |
ALS | Amyotrophic Lateral Sclerosis |
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Title | Lead | Aims | Sample Size | Imaging | Journal | Year |
---|---|---|---|---|---|---|
Using simultaneous PET/MRI to compare the accuracy of diagnosing frontotemporal dementia by arterial spin labeling MRI and FDG-PET | Anazodo et al. [11] | Compare MRI-arterial spin labeling (MRI-ASL) with FDG-PET in diagnosing frontotemporal dementia (FTD) | 10 FTD patients/10 HC | 18F-FDG PET/MRI on 3 T Siemens Biograph | NeuroImage: Clinical | 2018 |
The contribution of beta-amyloid to dementia in Lewy body diseases: a 1-year follow-up study | Biundo et al. [12] | Explore the contribution of Aß in Lewy body disease, especially in Parkinson’s disease patients with and without amyloid | 40 PD patients (13 with dementia, 22 MCI, 5 normal) and 10 DLB patients | 18F-Flutemetamol PET/MRI on 3 T Siemens Biograph mMR | Brain Communications | 2021 |
Association between lower body temperature and increased tau pathology in cognitively normal older adults | Blessing et al. [13] | Cross-sectionally evaluate the association between body temperature (as a proxy for brain temperature) and tau pathology in cognitively normal older adults using plasma and CSF P-tau181 and PET-MR | 21 patients | 18F-MK-6240 PET/MRI | Neurobiology of Disease | 2022 |
Support vector machine learning and diffusion-derived structural networks predict amyloid quantity and cognition in adults with Down’s syndrome | Brown et al. [14] | Assess the effectiveness of hybrid imaging to predict brain amyloid plaque burden, baseline cognition, and longitudinal cognitive change using support vector regression | 95 patients with Down’s syndrome | 11C-PiB PET/MRI on 3 T GE Signa | Neurobiology of Aging | 2022 |
Myelin imaging measures as predictors of cognitive impairment in MS patients: A hybrid PET-MRI study | Campanholo et al. [15] | Highlight differences in myelin imaging modalities that can be used as predictors of cognitive dysfunction in patients with multiple sclerosis (MS) | 51 MS patients/24 HC | 11C-PiB PET/MRI on GE Signa | Multiple Sclerosis and Related Disorders | 2022 |
Simultaneous FDG-PET/MRI detects hippocampal subfield metabolic differences in AD/MCI | Carlson et al. [16] | Study changes in FDG-PET and time-of-flight MRI (TOF-MRI) in Alzheimer’s disease, focusing on the hippocampus and its subregions | 9 AD and 6 MCI patients/17 HC | 18F-FDG PET/MRI on 3 T GE Signa | Scientific Reports | 2020 |
Hippocampal subfield imaging and fractional anisotropy show parallel changes in Alzheimer’s disease tau progression using simultaneous tau-PET/MRI at 3 T | Carlson et al. [17] | Examine the development of tau pathology on PET and its relationship with hippocampal connectivity changes on diffusion tensor imaging (DTI) | 5 AD and MCI patients/13 HC | 18F-PI-2620 PET/MRI on 3 T GE Signa | Alzheimer’s & Dementia (Amsterdam) | 2021 |
Direct prospective comparison of (18)F-FDG PET and arterial spin labeling MR using simultaneous PET/MR in patients referred for diagnosis of dementia | Ceccarini et al. [18] | Conduct a head-to-head comparison of FDG-PET and MRI-ASL in diagnosing cognitive impairment (Alzheimer’s disease [AD], Lewy Body Dementia [LBD], FTD) in patients with suspected cognitive impairment | 27 suspected CI patients/30 HC | 18F-FDG PET/MRI on GE Signa | European Journal of Nuclear Medicine and Molecular Imaging | 2020 |
Evaluating the association between brain atrophy, hypometabolism, and cognitive decline in Alzheimer’s disease: a PET/MRI study | Chen et al. [19] | Evaluate changes in the hippocampus and default mode network as biomarkers for the diagnosis of AD | 23 AD patients/24 HC | 18F-FDG PET/MRI on 3 T GE Signa | Aging (Albany NY) | 2021 |
Multiparametric hippocampal signatures for early diagnosis of Alzheimer’s disease using (18)F-FDG PET/MRI Radiomics | Chen et al. [20] | Explore the utility of hippocampal radiomic data to conduct early diagnosis of AD | 51 AD patients and 55 aMCI patients/53 HC | 18F-FDG PET/MRI on GE Signa | CNS Neuroscience & Therapeutics | 2023 |
Characterizing Differences in Functional Connectivity Between Posterior Cortical Atrophy and Semantic Dementia by Seed-Based Approach | Chen et al. [21] | Demonstrate the existence of abnormal functional connectivity (FC) with an unaffected network in posterior cortical atrophy (PCA) and semantic dementia (SD) using neuropsychological assessments and PET/MRI scans | 12 SD patients/11 HC | 18F-FDG PET/MRI on 3 T GE Signa | Frontiers in Aging Neuroscience | 2022 |
Glucose Hypometabolism in Hippocampal Subdivisions in Alzheimer’s Disease: A Pilot Study Using High-Resolution 18F-FDG PET and 7.0-T MRI | Choi et al. [22] | Compare the glucose metabolism of hippocampal divisions, a clinical diagnostic marker of AD, in mild-AD patients and healthy controls | 9 eAD patients/10 HC | 18F-FDG PET/MRI on 7 T Siemens HRRT-PET | Journal of Clinical Neurology | 2018 |
Investigating the Roles of Anterior Cingulate in Behavioral Variant Frontotemporal Dementia: A PET/MRI Study | Chu et al. [23] | Explore the role that the anterior cingulate cortex plays in behavioral deficits and executive dysfunction using hybrid imaging | 21 bvFTD patients/21 HC | 18F-FDG PET/MRI on 3 T GE Signa | Journal of Alzheimer’s Disease | 2021 |
Coupling relationship between glucose and oxygen metabolisms to differentiate preclinical Alzheimer’s disease and normal individuals | Ding et al. [24] | Explore the relationship between fMRI and FDG-PET signals in preclinical Alzheimer’s disease and Mild Cognitive Impairment (MCI), using biomarkers for early detection | 15 CI and 20 preAD patients/27 HC | 18F-FDG-PET/MRI and 18F-AV45-PET/MRI on 3 T GE Signa | Human Brain Mapping | 2021 |
Diffusion MRI biomarkers of white matter microstructure vary nonmonotonically with increasing cerebral amyloid deposition | Dong et al. [25] | Cross-sectionally characterize the pathological white matter changes in AD and mild cognitive impairment (MCI) using integrated PET/MR imaging, kurtosis imaging (DKI), and axonal water fraction (AWF) | 21 MCI or early AD patients/23 HC | 18F-FDG PET/MRI on 3 T Siemens Biograph mMR | Neurobiology of Aging | 2020 |
FDG PET/MRI for Visual Detection of Crossed Cerebellar Diaschisis in Patients With Dementia | Franceschi et al. [26] | To evaluate the presence of crossed cerebellar diaschisis in patients with suspected neurodegenerative disease | 75 patients with neurodegenerative disease | 18F-FDG PET/MRI on 3 T Siemens Biograph mMR | American Journal of Roentgenology | 2021 |
Hybrid imaging in dementia: A semi-quantitative ((18)F)-fluorodeoxyglucose positron emission tomography/magnetic resonance imaging approach in clinical practice | Franceschi et al. [27] | Retrospectively assess the relationship between semi-quantitative changes in lobar-specific gray matter volumes and corresponding regions of brain fluorodeoxyglucose (FDG) hypometabolism in patients with dementia and neurodegenerative disease using FDG PET/MRI, NeuroQuant morphometric analysis, and z-scores | 89 dementia patients | 18F-FDG PET/MRI on 3 T Siemens Biograph mMR | World Journal of Nuclear Medicine | 2020 |
((18)F)-Fluorodeoxyglucose positron emission tomography/magnetic resonance imaging assessment of hypometabolism patterns in clinical phenotypes of suspected corticobasal degeneration | Franceschi et al. [28] | Retrospectively evaluate the metabolic and volumetric abnormalities in patients with clinically suspected corticobasal degeneration (CBD) using FDG PET/MRI | 75 suspected CBD patients | 18F-FDG PET/MRI on 3 T Siemens Biograph mMR | World Journal of Nuclear Medicine | 2020 |
Metabolic positron-emission tomography/magnetic resonance imaging in primary progressive aphasia and frontotemporal lobar degeneration subtypes: Reassessment of expected [(18)F]-fluorodeoxyglucose uptake patterns | Franceschi et al. [29] | Evaluate FDG uptake patterns in patients with frontotemporal lobar degeneration/primary progressive aphasia (FTLD/PPA) subtypes | 51 FTLD/PPA patients | 18F-FDG PET/MRI on 3 T Siemens Biograph mMR | World Journal of Nuclear Medicine | 2021 |
Functional Abnormality Associated With Tau Deposition in Alzheimer’s Disease—A Hybrid Positron Emission Tomography/MRI Study | Fu et al. [30] | Investigate the characteristics of tau deposition and its impact on functional connectivity (FC) in AD using neuropsychological assessments and FDG PET/MRI scans | 26 AD patients/19 HC | 18F-THK5317 PET/MRI | Frontiers in Aging Neuroscience | 2021 |
Quantification of Brain β-Amyloid Load in Parkinson’s Disease With Mild Cognitive Impairment: A PET/MRI Study | Garon et al. [31] | Study how Aβ affects clinical presentation and regional brain volumes in PD-MCI | 25 PD-MCI patients | 18F-FDG PET/MRI on 3 T | Frontiers in Neurology | 2022 |
Reduced blood oxygenation level dependent connectivity is related to hypoperfusion in Alzheimer’s disease | Göttler et al. [32] | Investigate the relationship between functional connectivity in the posterior default mode network (pDMN) using resting-state fMRI blood oxygenation level-dependent signal fluctuations (BOLD-FC) and PET/MRI in patients with AD | 42 AD patients/27 HC | 18F-FDG PET/MRI on 3 T Siemens Biograph mMR | Journal of Cerebral Blood Flow and Metabolism | 2019 |
The 100-plus Study of cognitively healthy centenarians: rationale, design and cohort description | Holstege et al. [33] | Cohort study identifying characteristics associated with escape/delay of cognitive decline in centenarians enrolled in the 100-plus Study using MMSE tests, PET/MRI or PET/CT, feces collection, and post-mortem brain donation | 300 patients | Unspecified PET/MRI | European Journal of Epidemiology | 2018 |
Neuroimaging, clinical and life course correlates of normal-appearing white matter integrity in 70-year-olds | James et al. [34] | Explore how changes in normal-appearing white matter relate to brain health and modifiable lifestyle factors, considering confounders such as sex, white matter hyperintensity volume, and ApoE4 status | 502 patients | 18F-Florbetapir PET/MRI on Siemens Biograph mMR | Brain Communications | 2023 |
Adulthood cognitive trajectories over 26 years and brain health at 70 years of age: findings from the 1946 British Birth Cohort | James et al. [35] | Characterize individual changes in cognitive function through mid- and later life in relation to brain health measures using PET/MRI, amyloid PET, whole-brain volume, hippocampal volume, and white matter hyperintensity volume (WMHV) | 468 patients | 18F-FDG PET/MRI on 3 T Siemens Biograph mMR | Neurobiology of Aging | 2023 |
Hybrid FDG PET/MRI vs. FDG PET and CT in patients with suspected dementia—A comparison of diagnostic yield and propagated influence on clinical diagnosis and patient management | Kaltoft et al. [36] | Retrospectively compare simultaneous FDG-PET/MRI with PET/CT in identifying cognitive impairment features, evaluating the clinical impact of adding MRI to CT | 78 patients | 18F-FDG-PET on 3 T Siemens Biograph mMR | PLoS One | 2019 |
Prediction of Amyloid Positivity in Mild Cognitive Impairment Using Fully Automated Brain Segmentation Software | Kang et al. [37] | To score the predictive ability of regional volume information extracted from PET/MRI images using FreeSurfer for cerebral amyloid positivity in patients with MCI | 130 aMCI patients | 11C-PiB PET/MRI on 3 T Siemens Biograph mMR | Neuropsychiatric Disease and Treatment | 2020 |
Assessment of Alzheimer’s Disease Imaging Biomarkers in World Trade Center Responders with Cognitive Impairment at Midlife | Kritikos et al. [38] | Analyze preliminary results of FDG-PET and amyloid PET scans in World Trade Center first responders, assessing the risk of dementia | 6 CI and 6 MCI patients | 18F-FBB-PET and 18F-FTP-PET on 3 T Siemens Biograph mMR | World Journal of Nuclear Medicine | 2022 |
Estimation of brain amyloid accumulation using deep learning in clinical [(11)C]PiB PET imaging | Ladefoged et al. [39] | Develop a deep learning model for predicting SUVR and Amyloid Status in 11C PiB PET scans, using MRI in the test set | 1309 CI patients | 11C-PiB-PET/MRI | EJNMMI Physics | 2023 |
Tau-PET imaging predicts cognitive decline and brain atrophy progression in early Alzheimer’s disease | Lagarde et al. [40] | Explore regional tau binding measured at baseline is associated with AD progression over 2 years using PET/MRI and CSF biomarkers | 36 AD patients/15 HC | 18F-FDG PET/MRI on 3 T | Journal of Neurology, Neurosurgery, and Psychiatry | 2022 |
Reconfigured metabolism brain network in asymptomatic microtubule-associated protein tau mutation carriers: a graph theoretical analysis | Liu et al. [41] | Explore patterns of metabolism topology reconfiguration in microtubule-associated protein tau MAPT mutation carriers during presymptomatic stages of genetic frontotemporal dementia (FDT) using neuropsychological testing, genetic testing, and PET/MRI | 32 bvFTD/33 HC | 18F-FDG PET/MRI on 3 T GE Signa | Alzheimer’s Research & Therapy | 2022 |
Altered metabolic connectivity within the limbic cortico-striato-thalamo-cortical circuit in presymptomatic and symptomatic behavioral variant frontotemporal dementia | Liu et al. [42] | Characterize the metabolic connectivity between areas of the limbic cortico–striatal–thalamic–cortical (CSTC) circuit in presymptomatic and symptomatic bvFTD patients | 33 bvFTD patients/33 HC | 18F-FDG PET/MRI on 3 T GE Signa | Alzheimer’s Research & Therapy | 2023 |
Involvement of striatal motoric subregions in familial frontotemporal dementia with parkinsonism harboring the C9orf72 repeat expansions | Liu et al. [43] | Explore the roles of striatal motor subdivisions in the pathogenesis of parkinsonism resulting from C9ORF72 repeat expansions in patients with FTDP (frontotemporal dementia with parkinsonism) using PET/MRI and PET/CT | 2 FTDP patients/17 HC | 18F-FDG PET/MRI on 3 T GE Signa | NPJ Parkinson’s Disease | 2022 |
Visuomotor integration deficits are common to familial and sporadic preclinical Alzheimer’s disease | Lu et al. [44] | Investigate the discernibility of subtle visuomotor deficits in familial and sporadic preclinical AD using β-amyloid-PET/MRI, whole-brain volume, and white matter hyperintensity volume in presymptomatic familial AD patients | 31 FAD patients/390 HC | 18F-FDG PET/MRI on 3 T Siemens Biograph mMR | Brain Communications | 2021 |
Decoupling of regional neural activity and inter-regional functional connectivity in Alzheimer’s disease: a simultaneous PET/MR study | Maleki et al. [45] | Explore the effect of AD and MCI on the coupling between regional neural activity and inter-regional functional connectivity | 33 AD patients/26 HC | 18F-FDG PET/MRI on Siemens Biograph mMR | European Journal of Nuclear Medicine and Molecular Imaging | 2022 |
Hydrocephalic Dementia: Revisited with Multimodality Imaging and toward a Unified Imaging Approach | Mangalore et al. [46] | Study the correlation between normal pressure hydrocephalus and dementia, analyzing imaging findings and clinical symptoms | 13 NPH patients | 18F-FDG PET/MRI | Journal of Neuroscience in Rural Practice | 2021 |
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Cerebral Oxidative Stress in Early Alzheimer’s Disease Evaluated by (64)Cu-ATSM PET/MRI: A Preliminary Study | Okazawa et al. [50] | Evaluate the degree of oxidative stress and amyloid burden in the brains of AD patients | 10 eAD patients/10 HC | 64Cu-ATSM PET/MRI on 3 T GE Signa | Antioxidants (Basel) | 2022 |
Noninvasive Measurement of [(11)C]PiB Distribution Volume Using Integrated PET/MRI | Okazawa et al. [51] | Explore the utility of a non-invasive method for determining the arterial concentration of radioactive tracer in PET image reconstruction | 19 MCI patients/16 HC | 11C-PiB PET/MRI on GE Signa | Diagnostics (Basel) | 2020 |
Hippocampal subfield volumes and pre-clinical Alzheimer’s disease in 408 cognitively normal adults born in 1946 | Parker et al. [52] | Cross-sectionally analyze the relationship between cerebral β-amyloid deposition and volume of individual hippocampal subfields in cognitively normal older adults using MMSE, PET/MRI | 408 patients | 18F-FDG PET/MRI on 3 T Siemens Biograph mMR | PLoS One | 2019 |
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Decreased Alpha Peak Frequency Is Linked to Episodic Memory Impairment in Pathological Aging | Puttaert et al. [54] | Investigate the link between alpha brain activity and alterations in episodic memory as assessed by PET/MRI, FCSRT (Free and Cued Selective Reminding Test), and R-MEG (Resting-State Magnetoencephalography) | 37 AD patients/19 HC | 18F-FDG PET/MRI on 3 T GE Signa | Frontiers in Aging Neuroscience | 2021 |
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Simultaneous PET/fMRI Detects Distinctive Alterations in Functional Connectivity and Glucose Metabolism of Precuneus Subregions in Alzheimer’s Disease | Zhang et al. [70] | Explore the involvement of the precuneus in Alzheimer’s disease, focusing on glucose metabolism and functional connectivity | 20 AD and 23 MCI patients/27 HC | 18F-FDG PET/MRI on Siemens Biograph mMR | Frontiers in Aging Neuroscience | 2021 |
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Lee, J.; Renslo, J.; Wong, K.; Clifford, T.G.; Beutler, B.D.; Kim, P.E.; Gholamrezanezhad, A. Current Trends and Applications of PET/MRI Hybrid Imaging in Neurodegenerative Diseases and Normal Aging. Diagnostics 2024, 14, 585. https://doi.org/10.3390/diagnostics14060585
Lee J, Renslo J, Wong K, Clifford TG, Beutler BD, Kim PE, Gholamrezanezhad A. Current Trends and Applications of PET/MRI Hybrid Imaging in Neurodegenerative Diseases and Normal Aging. Diagnostics. 2024; 14(6):585. https://doi.org/10.3390/diagnostics14060585
Chicago/Turabian StyleLee, Jonathan, Jonathan Renslo, Kasen Wong, Thomas G. Clifford, Bryce D. Beutler, Paul E. Kim, and Ali Gholamrezanezhad. 2024. "Current Trends and Applications of PET/MRI Hybrid Imaging in Neurodegenerative Diseases and Normal Aging" Diagnostics 14, no. 6: 585. https://doi.org/10.3390/diagnostics14060585