Stage-Dependent Cerebral Blood Flow and Leukoaraiosis Couplings in Subcortical Ischemic Vascular Disease and Alzheimer’s Disease

Min-Chien Tu; Hsiao-Wen Chung; Yen-Hsuan Hsu; Jir-Jei Yang; Wen-Chau Wu

doi:10.3233/jad-215405

journal article Open Access Mar 22, 2022

Stage-Dependent Cerebral Blood Flow and Leukoaraiosis Couplings in Subcortical Ischemic Vascular Disease and Alzheimer’s Disease

Min-Chien Tu Hsiao-Wen Chung Yen-Hsuan Hsu Jir-Jei Yang Wen-Chau Wu

Journal of Alzheimer’s Disease Vol. 86 No. 2 pp. 729-739 · SAGE Publications

View at Publisher Save 10.3233/jad-215405

Abstract

Background: Alzheimer’s disease (AD) and subcortical ischemic vascular disease (SIVD) have both been associated with white matter hyperintensities (WMHs) and altered cerebral blood flow (CBF) although the etiology of AD is still unclear. Objective: To test the hypothesis that CBF and WMHs have differential effects on cognition and that the relationship between CBF and WMHs changes with the subtypes and stages of dementia. Methods: Forty-two patients with SIVD, 50 patients with clinically-diagnosed AD, and 30 cognitively-normal subjects were included. Based on the Clinical Dementia Rating (CDR), the patients were dichotomized into early-stage (CDR = 0.5) and late-stage (CDR = 1 or 2) groups. CBF and WMH metrics were derived from magnetic resonance imaging and correlated with cognition. Results: Hierarchical linear regression revealed that CBF metrics had distinct contribution to global cognition, memory, and attention, whereas WMH metrics had distinct contribution to executive function (all p < 0.05). In SIVD, the WMHs in frontotemporal areas correlated with the CBF in bilateral thalami at the early stage; the correlation then became between the WMHs in basal ganglia and the CBF in frontotemporal areas at the late stage. A similar corticosubcortical coupling was observed in AD but involved fewer areas. Conclusion: A stage-dependent coupling between CBF and WMHs was identified in AD and SIVD, where the extent of cortical WMHs correlated with subcortical CBF for CDR = 0.5, whereas the extent of subcortical WMHs correlated with cortical CBF for CDR = 1–2.

Topics

No keywords indexed for this article. Browse by subject →

References

50

[1]

Appelman "Total cerebral blood flow, white matter lesions and brain atrophy: The SMART-MR study" J Cereb Blood Flow Metab (2008) 10.1038/sj.jcbfm.9600563

[2]

Hainsworth "Do in vivo experimental models reflect human cerebral small vessel disease? A systematic review" J Cereb Blood Flow Metab (2008) 10.1038/jcbfm.2008.91

[3]

Prins "White matter hyperintensities, cognitive impairment and dementia: An update" Nat Rev Neurol (2015) 10.1038/nrneurol.2015.10

[4]

Johnson "Pattern of cerebral hypoperfusion in Alzheimer disease and mild cognitive impairment measured with arterial spin-labeling MR imaging: Initial experience" Radiology (2005) 10.1148/radiol.2343040197

[5]

Soldan "White matter hyperintensities and CSF Alzheimer disease biomarkers in preclinical Alzheimer disease" Neurology (2020) 10.1212/wnl.0000000000008864

[6]

Spatial patterns of white matter hyperintensities associated with Alzheimer’s disease risk factors in a cognitively healthy middle-aged cohort

Gemma Salvadó, Anna Brugulat-Serrat, Carole H. Sudre et al.

Alzheimer's Research & Therapy 2019 10.1186/s13195-018-0460-1

[7]

Damulina "White matter hyperintensities in Alzheimer’s disease: A lesion probability mapping study" J Alzheimers Dis (2019) 10.3233/jad-180982

[8]

Tubi "White matter hyperintensities and their relationship to cognition: Effects of segmentation algorithm" Neuroimage (2020) 10.1016/j.neuroimage.2019.116327

[9]

Rizzi "Global epidemiology of dementia: Alzheimer’s and vascular types" Biomed Res Int (2014) 10.1155/2014/908915

[10]

Hachinski "Cerebral blood flow in dementia" Arch Neurol (1975) 10.1001/archneur.1975.00490510088009

[11]

Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade

Clifford R Jack, David S Knopman, William J Jagust et al.

The Lancet Neurology 2010 10.1016/s1474-4422(09)70299-6

[12]

Zlokovic "Neurovascular pathways to neurodegeneration in Alzheimer’s disease and other disorders" Nat Rev Neurosci (2011) 10.1038/nrn3114

[13]

ElAli "Mild chronic cerebral hypoperfusion induces neurovascular dysfunction, triggering peripheral beta-amyloid brain entry and aggregation" Acta Neuropathol Commun (2013) 10.1186/2051-5960-1-75

[14]

Tu "Effectiveness of diffusion tensor imaging in differentiating early-stage subcortical ischemic vascular disease, Alzheimer’s disease and normal ageing" PloS One (2017) 10.1371/journal.pone.0175143

[15]

Shyu "Factor structure and explanatory variables of the Mini-Mental State Examination (MMSE) for elderly persons in Taiwan" J Formos Med Assoc (2001)

[16]

Erkinjuntti T , Inzitari D , Pantoni L , Wallin A , Scheltens P , Rockwood K , Roman G , Chui H , Desmond DW (2000) Research criteria for subcortical vascular dementia in clinical trials. In Advances in Dementia Research, Springer, pp. 23–30. 10.1007/978-3-7091-6781-6_4

[17]

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

Guy M. McKhann, David S. Knopman, Howard Chertkow et al.

Alzheimer's & Dementia 2011 10.1016/j.jalz.2011.03.005

[18]

Lin "[Cognitive Abilities Screening Instrument, Chinese Version 2.0 (CASI C-2.0): Administration and clinical application]" Acta Neurol Taiwan (2012)

[19]

Wang "Psychometric properties of the Taiwanese (traditional Chinese) version of the frontal assessment battery: A preliminary study" Appl Neuropsychol Adult (2016) 10.1080/23279095.2014.995792

[20]

Wechsler D (1997) Wechsler memory scale (WMS-III), Psychological Corporation, San Antonio, TX.

[21]

Hinton-Bayre "Comparability, reliability, and practice effects on alternate forms of the Digit Symbol Substitution and Symbol Digit Modalities tests" Psychol Assess (2005) 10.1037/1040-3590.17.2.237

[22]

Fan "Testing the efficiency and independence of attentional networks" J Cogn Neurosci (2002) 10.1162/089892902317361886

[23]

Anastasi A , Urbina S (1997) Psychological testing, Prentice Hall/Pearson Education.

[24]

Wu "Caffeine alters resting-state functional connectivity measured by blood oxygenation level-dependent MRI" NMR Biomed (2014) 10.1002/nbm.3080

[25]

Wahlund "A new rating scale for age-related white matter changes applicable to MRI and CT" Stroke (2001) 10.1161/01.str.32.6.1318

[26]

Sun "Cerebral blood flow alterations as assessed by 3D ASL in cognitive impairment in patients with subcortical vascular cognitive impairment: A marker for disease severity" Front Aging Neurosci (2016) 10.3389/fnagi.2016.00211

[27]

Firbank "Cerebral blood flow by arterial spin labeling in poststroke dementia" Neurology (2011) 10.1212/wnl.0b013e318217e76a

[28]

Bangen "Entorhinal perfusion predicts future memory decline, neurodegeneration, and white matter hyperintensity progression in older adults" J Alzheimers Dis (2021) 10.3233/jad-201474

[29]

Schuff "Cerebral blood flow in ischemic vascular dementia and Alzheimer’s disease, measured by arterial spin-labeling magnetic resonance imaging" Alzheimers Dement (2009) 10.1016/j.jalz.2009.04.1233

[30]

Camargo "Longitudinal cerebral blood flow changes in normal aging and the Alzheimer’s disease continuum identified by arterial spin labeling MRI" J Alzheimers Dis (2021) 10.3233/jad-210116

[31]

Duan "Cerebral blood flow is associated with diagnostic class and cognitive decline in Alzheimer’s disease" J Alzheimers Dis (2020) 10.3233/jad-200034

[32]

Mak "Quantitative assessment of cerebral hemodynamic parameters by QUASAR arterial spin labeling in Alzheimer’s disease and cognitively normal elderly adults at 3-tesla" J Alzheimers Dis (2012) 10.3233/jad-2012-111877

[33]

Hu "The right superior frontal gyrus and individual variation in proactive control of impulsive response" J Neurosci (2016) 10.1523/jneurosci.1175-16.2016

[34]

Sebastian "Dissociable attentional and inhibitory networks of dorsal and ventral areas of the right inferior frontal cortex: A combined task-specific and coordinate-based meta-analytic fMRI study" Brain Struct Funct (2016) 10.1007/s00429-015-0994-y

[35]

Shah-Basak "The role of the right superior temporal gyrus in stimulus-centered spatial processing" Neuropsychologia (2018) 10.1016/j.neuropsychologia.2018.03.027

[36]

Ding "Enhanced spontaneous functional connectivity of the superior temporal gyrus in early deafness" Sci Rep (2016) 10.1038/srep23239

[37]

Koyama "Differential contributions of the middle frontal gyrus functional connectivity to literacy and numeracy" Sci Rep (2017) 10.1038/s41598-017-17702-6

[38]

Stricker "Decreased white matter integrity in late-myelinating fiber pathways in Alzheimer’s disease supports retrogenesis" Neuroimage (2009) 10.1016/j.neuroimage.2008.11.027

[39]

Deoni "Cortical maturation and myelination in healthy toddlers and young children" Neuroimage (2015) 10.1016/j.neuroimage.2015.04.058

[40]

Huynh "CT perfusion quantification of small-vessel ischemic severity" AJNR Am J Neuroradiol (2008) 10.3174/ajnr.a1238

[41]

Van den Bergh "Centrifugal elements in the vascular pattern of the deep intracerebral blood supply" Angiology (1969) 10.1177/000331976902000205

[42]

Brozici "Anatomy and functionality of leptomeningeal anastomoses: A review" Stroke (2003) 10.1161/01.str.0000095791.85737.65

[43]

Charidimou "White matter hyperintensity patterns in cerebral amyloid angiopathy and hypertensive arteriopathy" Neurology (2016) 10.1212/wnl.0000000000002362

[44]

Wen "Effect of white matter changes on cognitive impairment in patients with lacunar infarcts" Stroke (2004) 10.1161/01.str.0000133686.29320.58

[45]

Saré "Diaschisis: An old concept brought to new life" J Neurosci (2016) 10.1523/jneurosci.4014-15.2016

[46]

In vivo staging of regional amyloid deposition

Michel J. Grothe, Henryk Barthel, Jorge Sepulcre et al.

Neurology 2017 10.1212/wnl.0000000000004643

[47]

Schöll "Biomarkers for tau pathology" Mol Cell Neurosci (2019) 10.1016/j.mcn.2018.12.001

[48]

Struyfs "Diffusion kurtosis imaging: A possible MRI biomarker for AD diagnosis?" J Alzheimers Dis (2015) 10.3233/jad-150253

[49]

Boespflug "Targeted assessment of enlargement of the perivascular space in Alzheimer’s disease and vascular dementia subtypes implicates astroglial involvement specific to Alzheimer’s disease" J Alzheimers Dis (2018) 10.3233/jad-180367

[50]

Van Gelderen "Pittfalls of MRI measurement of white matter perfusion based on arterial spin labeling" Magn Reson Med (2008) 10.1002/mrm.21515

Metrics

8

Citations

50

References

Details

Published: Mar 22, 2022
Vol/Issue: 86(2)
Pages: 729-739
License: View

Authors

M

Min-Chien Tu

Graduate Institute of Biomedical Electronics and Bioinformatics, National Taiwan University, Taipei, Taiwan; Department of Neurology, Taichung Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, Taichung, Taiwan; Department of Neurology, School of Medicine, Tzu Chi University, Hualien

H

Hsiao-Wen Chung

Graduate Institute of Biomedical Electronics and Bioinformatics, National Taiwan University, Taipei, Taiwan

Y

Yen-Hsuan Hsu

Department of Psychology, National Chung Cheng University, Chiayi, Taiwan; Center for Innovative Research on Aging Society, National Chung Cheng University, Chiayi, Taiwan

J

Jir-Jei Yang

Department of Radiology, Taichung Tzu Chi Hospital, Buddhist Tzu Chi Medical Foundation, Taichung, Taiwan

W

Wen-Chau Wu

Graduate Institute of Biomedical Electronics and Bioinformatics, National Taiwan University, Taipei, Taiwan; Institute of Medical Device and Imaging, National Taiwan University, Taipei, Taiwan

Cite This Article

Min-Chien Tu, Hsiao-Wen Chung, Yen-Hsuan Hsu, et al. (2022). Stage-Dependent Cerebral Blood Flow and Leukoaraiosis Couplings in Subcortical Ischemic Vascular Disease and Alzheimer’s Disease. Journal of Alzheimer’s Disease, 86(2), 729-739. https://doi.org/10.3233/jad-215405

Stage-Dependent Cerebral Blood Flow and Leukoaraiosis Couplings in Subcortical Ischemic Vascular Disease and Alzheimer’s Disease

You May Also Like