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Association of Arterial Spin Labeling Parameters With Cognitive Decline, Vascular Events, and Mortality in a Memory-Clinic Sample

      Highlights

      • What is the primary question addressed by this study?
        To investigate the association between arterial spin labelling (ASL) parameters [cerebral blood flow (CBF) and spatial coefficient of variation (sCoV)] and clinical outcomes in a memory clinic population.
      • What is the main finding of this study?
        Higher baseline gray matter-sCoV was associated with a decline in the memory domain over 3 years of follow-up.
        Participants with higher baseline gray matter-sCoV were at increased risk of vascular events.
      • What is the meaning of the finding?
        This indicates that the cerebrovascular insufficiency may lead to accelerated cognitive decline and worse clinical outcomes in memory clinic participants.

      Abstract

      Background

      Cognitive decline in older adults has been attributed to reduced cerebral blood flow (CBF). Recently, the spatial coefficient of variation (sCoV) of ASL has been proposed as a proxy marker of cerebrovascular insufficiency. We investigated the association between baseline ASL parameters with cognitive decline, incident cerebrovascular disease, and risk of vascular events and mortality.

      Design, Setting, and Participants

      About 368 memory-clinic patients underwent three-annual neuropsychological assessments and brain MRI scans at baseline and follow-up. MRIs were graded for white matter hyperintensities (WMH), lacunes, cerebral microbleeds (CMBs), cortical infarcts, and intracranial stenosis. Baseline gray (GM) and white matter (WM) CBF and GM-sCoV were obtained with ExploreASL from 2D-EPI pseudo-continuous ASL images. Cognitive assessment was done using a validated neuropsychological battery. Data on incident vascular events (heart disease, stroke, transient ischemic attack) and mortality were obtained.

      Results

      Higher baseline GM-sCoV was associated with decline in the memory domain over 3 years of follow-up. Furthermore, higher GM-sCoV was associated with a decline in the memory domain only in participants without dementia. Higher baseline GM-sCoV was associated with progression of WMH and incident CMBs. During a mean follow-up of 3 years, 29 (7.8%) participants developed vascular events and 18 (4.8%) died. Participants with higher baseline mean GM-sCoV were at increased risk of vascular events.

      Conclusions

      Higher baseline GM-sCoV of ASL was associated with a decline in memory and risk of cerebrovascular disease and vascular events, suggesting that cerebrovascular insufficiency may contribute to accelerated cognitive decline and worse clinical outcomes in memory clinic participants.

      Key Words

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      References

        • Chao LL
        • Buckley ST
        • Kornak J
        • et al.
        ASL perfusion MRI predicts cognitive decline and conversion from MCI to dementia.
        Alzheimer Dis Assoc Disord. 2010; 24: 19-27
        • De Vis JB
        • Peng SL
        • Chen X
        • et al.
        Arterial-spin-labeling (ASL) perfusion MRI predicts cognitive function in elderly individuals: a 4-year longitudinal study.
        J Magn Reson Imaging. 2018; 48: 449-458
        • Saridin FN
        • Hilal S
        • Villaraza SG
        • et al.
        Brain amyloid β, cerebral small vessel disease, and cognition. A memory clinic study.
        Neurology. 2020; 95: e2845-e2853
        • Gyanwali B
        • Shaik MA
        • Tan CS
        • et al.
        Mixed-location cerebral microbleeds as a biomarker of neurodegeneration in a memory clinic population.
        Aging. 2019; 11: 10581-10596
        • Petcharunpaisan S
        • Ramalho J
        • Castillo M.
        Arterial spin labeling in neuroimaging.
        World J Radiol. 2010; 2: 384-398
        • Mutsaerts HJ
        • Petr J
        • Václavů L
        • et al.
        The spatial coefficient of variation in arterial spin labeling cerebral blood flow images.
        J Cereb Blood Flow Metab. 2017; 37: 3184-3192
        • Juttukonda MR
        • Li B
        • Almaktoum R
        • et al.
        Characterizing cerebral hemodynamics across the adult lifespan with arterial spin labeling MRI data from the Human Connectome Project-Aging.
        Neuroimage. 2021; 230117807
        • Ferro DA
        • Mutsaerts HJ
        • Hilal S
        • et al.
        Cortical microinfarcts in memory clinic patients are associated with reduced cerebral perfusion.
        J Cereb Blood Flow Metab. 2020; 40: 1869-1878
        • Gyanwali B
        • Lai MKP
        • Lui B
        • et al.
        Blood-based cardiac biomarkers and the risk of cognitive decline, cerebrovascular disease, and clinical events.
        Stroke. 2021; 52: 2275-2283
        • TWHO MONICA Project Principal Investigators
        The World Health Organization MONICA Project (monitoring trends and determinants in cardiovascular disease): a major international collaboration.
        J Clin Epidemiol. 1988; 41: 105-114
        • Wardlaw JM
        • Smith EE
        • Biessels GJ
        • et al.
        Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration.
        Lancet Neurol. 2013; 12: 822-838
        • Hilal S
        • Mutsaerts H
        • Ferro D
        • et al.
        The effects of intracranial stenosis on cerebral perfusion and cognitive performance.
        J Alzheimers Dis. 2021; 79: 1-12
        • Alsop DC
        • Detre JA
        • Golay X
        • et al.
        Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia.
        Mag Reson Med. 2015; 73: 102-116
        • Mutsaerts H
        • Petr J
        • Groot P
        • et al.
        ExploreASL: an image processing pipeline for multi-center ASL perfusion MRI studies.
        Neuroimage. 2020; 219117031
        • MacIntosh BJ
        • Swardfager W
        • Robertson AD
        • et al.
        Regional cerebral arterial transit time hemodynamics correlate with vascular risk factors and cognitive function in men with coronary artery disease.
        Am J Neuroradiol. 2015; 36: 295-301
        • Tatu L
        • Moulin T
        • Vuillier F
        • et al.
        Arterial territories of the human brain.
        Front Neurol Neurosci. 2012; 30: 99-110
        • Sierra-Marcos A.
        Regional cerebral blood flow in mild cognitive impairment and alzheimer's disease measured with arterial spin labeling magnetic resonance imaging.
        Int J Alzheimers Dis. 2017; 20175479597
        • Heringa SM
        • Reijmer YD
        • Leemans A
        • et al.
        Multiple microbleeds are related to cerebral network disruptions in patients with early Alzheimer's disease.
        J Alzheimers Dis. 2014; 38: 211-221
        • Akoudad S
        • de Groot M
        • Koudstaal PJ
        • et al.
        Cerebral microbleeds are related to loss of white matter structural integrity.
        Neurology. 2013; 81: 1930-1937
        • Ding J
        • Sigurðsson S
        • Jónsson PV
        • et al.
        Space and location of cerebral microbleeds, cognitive decline, and dementia in the community.
        Neurology. 2017; 88: 2089-2097
        • Yew B
        • Nation DA
        • Alzheimer's Disease Neuroimaging I
        Cerebrovascular resistance: effects on cognitive decline, cortical atrophy, and progression to dementia.
        Brain. 2017; 140: 1987-2001
        • Zhao Y
        • Gong CX.
        From chronic cerebral hypoperfusion to Alzheimer-like brain pathology and neurodegeneration.
        Cell Mol Neurobiol. 2015; 35: 101-110
        • Wirth M
        • Pichet Binette A
        • Brunecker P
        • et al.
        Divergent regional patterns of cerebral hypoperfusion and gray matter atrophy in mild cognitive impairment patients.
        J Cereb Blood Flow Metab. 2017; 37: 814-824
        • Gorbach T
        • Pudas S
        • Lundquist A
        • et al.
        Longitudinal association between hippocampus atrophy and episodic-memory decline.
        Neurobiol Aging. 2017; 51: 167-176
        • Rusinek H
        • Brys M
        • Glodzik L
        • et al.
        Hippocampal blood flow in normal aging measured with arterial spin labeling at 3T.
        Magn Reson Med. 2011; 65: 128-137
        • Jahn H.
        Memory loss in Alzheimer's disease.
        Dialogues Clin Neurosci. 2013; 15: 445-454
        • Mortamais M
        • Artero S
        • Ritchie K
        Cerebral white matter hyperintensities in the prediction of cognitive decline and incident dementia.
        Int Rev Psychiatry. 2013; 25: 686-698
        • Bertsch K
        • Hagemann D
        • Hermes M
        • et al.
        Resting cerebral blood flow, attention, and aging.
        Brain Res. 2009; 1267: 77-88
        • van Osch MJ
        • Teeuwisse WM
        • van Walderveen MA
        • et al.
        Can arterial spin labeling detect white matter perfusion signal?.
        Magn Reson Med. 2009; 62: 165-173
        • Gyanwali B
        • Shaik MA
        • Tan BY
        • et al.
        Risk factors for and clinical relevance of incident and progression of cerebral small vessel disease markers in an Asian memory clinic population.
        J Alzheimers Dis. 2019; 67: 1209-1219
        • Sabayan B
        • van der Grond J
        • et al.
        Total cerebral blood flow and mortality in old age: a 12-year follow-up study.
        Neurology. 2013; 81: 1922-1929
        • Jefferson AL.
        Cardiac output as a potential risk factor for abnormal brain aging.
        J Alzheimers Dis. 2010; 20: 813-821
        • Alosco ML
        • Gunstad J
        • Jerskey BA
        • et al.
        The adverse effects of reduced cerebral perfusion on cognition and brain structure in older adults with cardiovascular disease.
        Brain Behav. 2013; 3: 626-636
        • van den Brule JMD
        • van der Hoeven JG
        • Hoedemaekers CWE.
        Cerebral perfusion and cerebral autoregulation after cardiac arrest.
        Biomed Res Int. 2018; 20184143636
        • Abizaid A
        • Horvath TL.
        Brain circuits regulating energy homeostasis.
        Regul Pept. 2008; 149: 3-10
        • Madero M
        • Gul A
        • Sarnak MJ
        Cognitive function in chronic kidney disease.
        Semin Dial. 2008; 21: 29-37