Magnetic Resonance Images Implicate That Glymphatic Alterations Mediate Cognitive Dysfunction in Alzheimer Disease
Objective The glymphatic system cleans amyloid and tau proteins from the brain in animal studies of Alzheimer disease (AD). However, there is no direct evidence showing this in humans. Methods Participants (n = 50, 62.6 ± 5.4 years old, 36 women) with AD and normal controls underwent amyloid positro...
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| Published in | Annals of neurology Vol. 93; no. 1; pp. 164 - 174 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Hoboken, USA
John Wiley & Sons, Inc
01.01.2023
Wiley Subscription Services, Inc |
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| Abstract | Objective
The glymphatic system cleans amyloid and tau proteins from the brain in animal studies of Alzheimer disease (AD). However, there is no direct evidence showing this in humans.
Methods
Participants (n = 50, 62.6 ± 5.4 years old, 36 women) with AD and normal controls underwent amyloid positron emission tomography (PET), tau PET, structural T1‐weighted magnetic resonance imaging, and neuropsychological evaluation. Whole‐brain glymphatic activity was measured by diffusion tensor image analysis along the perivascular space (DTI‐ALPS).
Results
ALPS‐indexes showed negative correlations with deposition of amyloid and tau on PET images and positive correlations with cognitive scores even after adjusting for age, sex, years of education, and APOE4 genotype covariates in multiple AD‐related brain regions (all p < 0.05). Mediation analysis showed that ALPS‐index acted as a significant mediator between regional standardized uptake value ratios of amyloid and tau images and cognitive dysfunction even after correcting for multiple covariates in AD‐related brain regions. These regions are responsible for attention, memory, and executive function, which are vulnerable to sleep deprivation.
Interpretation
Glymphatic system activity may act as a significant mediator in AD‐related cognitive dysfunction even after adjusting for multiple covariates and gray matter volumes. ALPS‐index may provide useful disease progression or treatment biomarkers for patients with AD as an indicator of modulation of glymphatic activity. ANN NEUROL 2023;93:164–174 |
|---|---|
| AbstractList | Objective
The glymphatic system cleans amyloid and tau proteins from the brain in animal studies of Alzheimer disease (AD). However, there is no direct evidence showing this in humans.
Methods
Participants (n = 50, 62.6 ± 5.4 years old, 36 women) with AD and normal controls underwent amyloid positron emission tomography (PET), tau PET, structural T1‐weighted magnetic resonance imaging, and neuropsychological evaluation. Whole‐brain glymphatic activity was measured by diffusion tensor image analysis along the perivascular space (DTI‐ALPS).
Results
ALPS‐indexes showed negative correlations with deposition of amyloid and tau on PET images and positive correlations with cognitive scores even after adjusting for age, sex, years of education, and APOE4 genotype covariates in multiple AD‐related brain regions (all p < 0.05). Mediation analysis showed that ALPS‐index acted as a significant mediator between regional standardized uptake value ratios of amyloid and tau images and cognitive dysfunction even after correcting for multiple covariates in AD‐related brain regions. These regions are responsible for attention, memory, and executive function, which are vulnerable to sleep deprivation.
Interpretation
Glymphatic system activity may act as a significant mediator in AD‐related cognitive dysfunction even after adjusting for multiple covariates and gray matter volumes. ALPS‐index may provide useful disease progression or treatment biomarkers for patients with AD as an indicator of modulation of glymphatic activity. ANN NEUROL 2023;93:164–174 The glymphatic system cleans amyloid and tau proteins from the brain in animal studies of Alzheimer disease (AD). However, there is no direct evidence showing this in humans. Participants (n = 50, 62.6 ± 5.4 years old, 36 women) with AD and normal controls underwent amyloid positron emission tomography (PET), tau PET, structural T1-weighted magnetic resonance imaging, and neuropsychological evaluation. Whole-brain glymphatic activity was measured by diffusion tensor image analysis along the perivascular space (DTI-ALPS). ALPS-indexes showed negative correlations with deposition of amyloid and tau on PET images and positive correlations with cognitive scores even after adjusting for age, sex, years of education, and APOE4 genotype covariates in multiple AD-related brain regions (all p < 0.05). Mediation analysis showed that ALPS-index acted as a significant mediator between regional standardized uptake value ratios of amyloid and tau images and cognitive dysfunction even after correcting for multiple covariates in AD-related brain regions. These regions are responsible for attention, memory, and executive function, which are vulnerable to sleep deprivation. Glymphatic system activity may act as a significant mediator in AD-related cognitive dysfunction even after adjusting for multiple covariates and gray matter volumes. ALPS-index may provide useful disease progression or treatment biomarkers for patients with AD as an indicator of modulation of glymphatic activity. ANN NEUROL 2023;93:164-174. The glymphatic system cleans amyloid and tau proteins from the brain in animal studies of Alzheimer disease (AD). However, there is no direct evidence showing this in humans.OBJECTIVEThe glymphatic system cleans amyloid and tau proteins from the brain in animal studies of Alzheimer disease (AD). However, there is no direct evidence showing this in humans.Participants (n = 50, 62.6 ± 5.4 years old, 36 women) with AD and normal controls underwent amyloid positron emission tomography (PET), tau PET, structural T1-weighted magnetic resonance imaging, and neuropsychological evaluation. Whole-brain glymphatic activity was measured by diffusion tensor image analysis along the perivascular space (DTI-ALPS).METHODSParticipants (n = 50, 62.6 ± 5.4 years old, 36 women) with AD and normal controls underwent amyloid positron emission tomography (PET), tau PET, structural T1-weighted magnetic resonance imaging, and neuropsychological evaluation. Whole-brain glymphatic activity was measured by diffusion tensor image analysis along the perivascular space (DTI-ALPS).ALPS-indexes showed negative correlations with deposition of amyloid and tau on PET images and positive correlations with cognitive scores even after adjusting for age, sex, years of education, and APOE4 genotype covariates in multiple AD-related brain regions (all p < 0.05). Mediation analysis showed that ALPS-index acted as a significant mediator between regional standardized uptake value ratios of amyloid and tau images and cognitive dysfunction even after correcting for multiple covariates in AD-related brain regions. These regions are responsible for attention, memory, and executive function, which are vulnerable to sleep deprivation.RESULTSALPS-indexes showed negative correlations with deposition of amyloid and tau on PET images and positive correlations with cognitive scores even after adjusting for age, sex, years of education, and APOE4 genotype covariates in multiple AD-related brain regions (all p < 0.05). Mediation analysis showed that ALPS-index acted as a significant mediator between regional standardized uptake value ratios of amyloid and tau images and cognitive dysfunction even after correcting for multiple covariates in AD-related brain regions. These regions are responsible for attention, memory, and executive function, which are vulnerable to sleep deprivation.Glymphatic system activity may act as a significant mediator in AD-related cognitive dysfunction even after adjusting for multiple covariates and gray matter volumes. ALPS-index may provide useful disease progression or treatment biomarkers for patients with AD as an indicator of modulation of glymphatic activity. ANN NEUROL 2023;93:164-174.INTERPRETATIONGlymphatic system activity may act as a significant mediator in AD-related cognitive dysfunction even after adjusting for multiple covariates and gray matter volumes. ALPS-index may provide useful disease progression or treatment biomarkers for patients with AD as an indicator of modulation of glymphatic activity. ANN NEUROL 2023;93:164-174. ObjectiveThe glymphatic system cleans amyloid and tau proteins from the brain in animal studies of Alzheimer disease (AD). However, there is no direct evidence showing this in humans.MethodsParticipants (n = 50, 62.6 ± 5.4 years old, 36 women) with AD and normal controls underwent amyloid positron emission tomography (PET), tau PET, structural T1‐weighted magnetic resonance imaging, and neuropsychological evaluation. Whole‐brain glymphatic activity was measured by diffusion tensor image analysis along the perivascular space (DTI‐ALPS).ResultsALPS‐indexes showed negative correlations with deposition of amyloid and tau on PET images and positive correlations with cognitive scores even after adjusting for age, sex, years of education, and APOE4 genotype covariates in multiple AD‐related brain regions (all p < 0.05). Mediation analysis showed that ALPS‐index acted as a significant mediator between regional standardized uptake value ratios of amyloid and tau images and cognitive dysfunction even after correcting for multiple covariates in AD‐related brain regions. These regions are responsible for attention, memory, and executive function, which are vulnerable to sleep deprivation.InterpretationGlymphatic system activity may act as a significant mediator in AD‐related cognitive dysfunction even after adjusting for multiple covariates and gray matter volumes. ALPS‐index may provide useful disease progression or treatment biomarkers for patients with AD as an indicator of modulation of glymphatic activity. ANN NEUROL 2023;93:164–174 |
| Author | Lin, Kun‐Ju Hsu, Jung‐Lung Wei, Yi‐Chia Hsiao, Ing‐Tsung Ro, Long‐Sun Yen, Tzu‐Chen Liao, Ming‐Feng Toh, Cheng Hong |
| AuthorAffiliation | 1 Department of Neurology New Taipei Municipal TuCheng Hospital New Taipei City Taiwan 8 Department of Nuclear Medicine and Center for Advanced Molecular Imaging and Translation Linkou Chang Gung Memorial Hospital Taoyuan Taiwan 2 Department of Neurology, Chang Gung Memorial Hospital Linkou Medical Center Neuroscience Research Center, and College of Medicine Chang‐Gung University Taoyuan Taiwan 3 Taipei Medical University Graduate Institute of Humanities in Medicine and Research Center for Brain and Consciousness, Shuang Ho Hospital Taipei Taiwan 4 Department of Neurology Chang Gung Memorial Hospital Keelung Taiwan 6 Institute of Neuroscience National Yang Ming Chiao Tung University Taipei Taiwan 7 Department of Medical Imaging and Intervention, Chang Gung Memorial Hospital at Linkou Chang Gung University College of Medicine Taoyuan Taiwan 10 APRINOIA Therapeutics Taipei Taiwan 5 Community Medicine Research Center Chang Gung Memorial Hospital Keelung Taiwan 9 Department of Medical Imaging and R |
| AuthorAffiliation_xml | – name: 6 Institute of Neuroscience National Yang Ming Chiao Tung University Taipei Taiwan – name: 2 Department of Neurology, Chang Gung Memorial Hospital Linkou Medical Center Neuroscience Research Center, and College of Medicine Chang‐Gung University Taoyuan Taiwan – name: 7 Department of Medical Imaging and Intervention, Chang Gung Memorial Hospital at Linkou Chang Gung University College of Medicine Taoyuan Taiwan – name: 8 Department of Nuclear Medicine and Center for Advanced Molecular Imaging and Translation Linkou Chang Gung Memorial Hospital Taoyuan Taiwan – name: 9 Department of Medical Imaging and Radiological Sciences and Healthy Aging Research Center Chang Gung University Taoyuan Taiwan – name: 4 Department of Neurology Chang Gung Memorial Hospital Keelung Taiwan – name: 1 Department of Neurology New Taipei Municipal TuCheng Hospital New Taipei City Taiwan – name: 3 Taipei Medical University Graduate Institute of Humanities in Medicine and Research Center for Brain and Consciousness, Shuang Ho Hospital Taipei Taiwan – name: 5 Community Medicine Research Center Chang Gung Memorial Hospital Keelung Taiwan – name: 10 APRINOIA Therapeutics Taipei Taiwan |
| Author_xml | – sequence: 1 givenname: Jung‐Lung orcidid: 0000-0001-6422-8870 surname: Hsu fullname: Hsu, Jung‐Lung organization: Graduate Institute of Humanities in Medicine and Research Center for Brain and Consciousness, Shuang Ho Hospital – sequence: 2 givenname: Yi‐Chia surname: Wei fullname: Wei, Yi‐Chia organization: National Yang Ming Chiao Tung University – sequence: 3 givenname: Cheng Hong orcidid: 0000-0002-8871-5101 surname: Toh fullname: Toh, Cheng Hong organization: Chang Gung University College of Medicine – sequence: 4 givenname: Ing‐Tsung surname: Hsiao fullname: Hsiao, Ing‐Tsung organization: Chang Gung University – sequence: 5 givenname: Kun‐Ju surname: Lin fullname: Lin, Kun‐Ju organization: Chang Gung University – sequence: 6 givenname: Tzu‐Chen surname: Yen fullname: Yen, Tzu‐Chen organization: APRINOIA Therapeutics – sequence: 7 givenname: Ming‐Feng surname: Liao fullname: Liao, Ming‐Feng organization: Chang‐Gung University – sequence: 8 givenname: Long‐Sun surname: Ro fullname: Ro, Long‐Sun email: cgrols@adm.cgmh.org.tw organization: Chang‐Gung University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36214568$$D View this record in MEDLINE/PubMed |
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| PublicationTitle | Annals of neurology |
| PublicationTitleAlternate | Ann Neurol |
| PublicationYear | 2023 |
| Publisher | John Wiley & Sons, Inc Wiley Subscription Services, Inc |
| Publisher_xml | – name: John Wiley & Sons, Inc – name: Wiley Subscription Services, Inc |
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The glymphatic system cleans amyloid and tau proteins from the brain in animal studies of Alzheimer disease (AD). However, there is no direct... The glymphatic system cleans amyloid and tau proteins from the brain in animal studies of Alzheimer disease (AD). However, there is no direct evidence showing... ObjectiveThe glymphatic system cleans amyloid and tau proteins from the brain in animal studies of Alzheimer disease (AD). However, there is no direct evidence... |
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| SubjectTerms | Aged Alzheimer Disease - pathology Alzheimer's disease Amyloid Amyloid - metabolism Animal diseases Biomarkers Brain Brain - pathology Cognitive ability Cognitive Dysfunction - pathology Executive function Female Genotypes Humans Image analysis Image processing Magnetic Resonance Imaging Male Medical imaging Middle Aged Neurodegenerative diseases Neuroimaging Positron emission Positron emission tomography Positron-Emission Tomography - methods Resonance Sleep deprivation Substantia grisea Tau protein tau Proteins - metabolism Tensors |
| Title | Magnetic Resonance Images Implicate That Glymphatic Alterations Mediate Cognitive Dysfunction in Alzheimer Disease |
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