Differentiation of Alzheimer’s Disease from Frontotemporal Dementia and Mild Cognitive Impairment Based on Arterial Spin Labeling Magnetic Resonance Imaging: A Pilot Cross-Sectional Study from PUMCH Dementia Cohort
Restricted accessResearch articleFirst published online May 16, 2023
Differentiation of Alzheimer’s Disease from Frontotemporal Dementia and Mild Cognitive Impairment Based on Arterial Spin Labeling Magnetic Resonance Imaging: A Pilot Cross-Sectional Study from PUMCH Dementia Cohort
Arterial spin labeling (ASL) is helpful in early diagnosis and differential diagnosis of Alzheimer’s disease (AD), with advantages including no exposure to radioactivity, no injection of a contrast agent, more accessible, and relatively less expensive.
Objective:
To establish the perfusion pattern of different dementia in Chinese population and evaluate the effectiveness of ASL in differentiating AD from cognitive unimpaired (CU), mild cognitive impairment (MCI), and frontotemporal dementia (FTD).
Methods:
Four groups of participants were enrolled, including AD, FTD, MCI, and CU based on clinical diagnosis from PUMCH dementia cohort. ASL image was collected using 3D spiral fast spin echo–based pseudo-continuous ASL pulse sequence with background suppression and a high resolution T1-weighted scan covering the whole brain. Data processing was performed using Dr. Brain Platform to get cerebral blood flow (ml/100g/min) in every region of interest cortices.
Results:
Participants included 66 AD, 26 FTD, 21 MCI, and 21 CU. Statistically, widespread hypoperfusion neocortices, most significantly in temporal-parietal-occipital cortices, but not hippocampus and subcortical nucleus were found in AD. Hypoperfusion in parietal lobe was most significantly associated with cognitive decline in AD. Hypoperfusion in parietal lobe was found in MCI and extended to adjacent temporal, occipital and posterior cingulate cortices in AD. Significant reduced perfusion in frontal and temporal cortices, including subcortical nucleus and anterior cingulate cortex were found in FTD. Hypoperfusion regions were relatively symmetrical in AD and left predominant especially in FTD.
Conclusion:
Specific patterns of ASL hypoperfusion were helpful in differentiating AD from CU, MCI, and FTD.
Graff-RadfordJ, YongKXX, ApostolovaLG, BouwmanFH, CarrilloM, DickersonBC, RabinoviciGD, SchottJM, JonesDT, MurrayME (2021) New insights into atypical Alzheimer’s disease in the era of biomarkers, Lancet Neurol20, 222–234.
DuAT, JahngGH, HayasakaS, KramerJH, RosenHJ, Gorno-TempiniML, RankinKP, MillerBL, WeinerMW, SchuffN (2006) Hypoperfusion in frontotemporal dementia and Alzheimer disease by arterial spin labeling MRI, Neurology67, 1215–1220.
6.
WolkDA, DetreJA (2012) Arterial spin labeling MRI: An emerging biomarker for Alzheimer’s disease and other neurodegenerative conditions, Curr Opin Neurol25, 421–428.
7.
GradeM, Hernandez TamamesJA, PizziniFB, AchtenE, GolayX, SmitsM (2015) A neuroradiologist’s guide to arterial spin labeling MRI in clinical practice, Neuroradiology57, 1181–1202.
8.
WeytsK, VernooijM, SteketeeR, ValkemaR, SmitsM (2017) Qualitative agreement and diagnostic performance of arterial spin labelling MRI and FDG PET-CT in suspected early-stage dementia: Comparison of arterial spin labelling MRI and FDG PET-CT in suspected dementia, Clin Imaging45, 1–7.
9.
HallerS, ZaharchukG, ThomasDL, LovbladKO, BarkhofF, GolayX (2016) Arterial spin labeling perfusion of the 569
brain: Emerging clinical applications. Radiology281, 337–356.
10.
ZhangN, GordonML, GoldbergTE (2017) Cerebral blood flow measured by arterial spin labeling MRI at resting state in normal aging and Alzheimer’s disease, Neurosci Biobehav Rev72, 168–175.
11.
AlsopDC, DaiW, GrossmanM, DetreJA (2010) Arterial spin labeling blood flow MRI: Its role in the early characterization of Alzheimer’s disease, J Alzheimers Dis20, 871–880.
DaiW, LopezOL, CarmichaelOT, BeckerJT, KullerLH, GachHM (2009) Mild cognitive impairment and alzheimer disease: Patterns of altered cerebral blood flow at MR imaging, Radiology250, 856–866.
14.
WierengaCE, HaysCC, ZlatarZZ (2014) Cerebral blood flow measuredby arterial spin labeling MRI as a preclinical marker of Alzheimer’sdisease, J Alzheimers Dis42(Suppl 4), S411–S419.
15.
McKhannGM, KnopmanDS, ChertkowH, HymanBT, JackCRJr., KawasCH, KlunkWE, KoroshetzWJ, ManlyJJ, MayeuxR, MohsRC, MorrisJC, RossorMN, ScheltensP, CarrilloMC, ThiesB, WeintraubS, PhelpsCH (2011) 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, Alzheimers Dement7, 263–269.
16.
McKhannGM, AlbertMS, GrossmanM, MillerB, DicksonD, TrojanowskiJQ (2001) Clinical and pathological diagnosis of frontotemporal dementia: Report of the Work Group on Frontotemporal Dementia and Pick’s Disease, Arch Neurol58, 1803–1809.
17.
AlbertMS, DeKoskyST, DicksonD, DuboisB, FeldmanHH, FoxNC, GamstA, HoltzmanDM, JagustWJ, PetersenRC, SnyderPJ, CarrilloMC, ThiesB, PhelpsCH (2011) The diagnosis of mild cognitive impairment due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease, Alzheimers Dement7, 270–279.
18.
TanJP, LiN, GaoJ, WangLN, ZhaoYM, YuBC, DuW, ZhangWJ, CuiLQ, WangQS, LiJJ, YangJS, YuJM, XiaXN, ZhouPY (2015) Optimal cutoff scores for dementia and mild cognitive impairment of the Montreal Cognitive Assessment among elderly and oldest-old Chinese population, J Alzheimers Dis43, 1403–1412.
19.
ZhangY, DouW, ZuoZ, YouH, LvY, HouB, ShiL, FengF (2021) Brain volume and perfusion asymmetry in temporal lobe epilepsy with and without hippocampal sclerosis, Neurol Res43, 299–306.
20.
BuxtonRB, UludağK, DubowitzDJ, LiuTT (2004) Modeling the hemodynamic response to brain activation, Neuroimage23 Suppl 1, S220–233.
21.
De VisJB, PengSL, ChenX, LiY, LiuP, SurS, RodrigueKM, ParkDC, LuH (2018) Arterial-spin-labeling (ASL) perfusion MRI predicts cognitive function in elderly individuals: A 4-year longitudinal study, J Magn Reson Imaging48, 449–458.
22.
AlsopDC, DetreJA, GrossmanM (2000) Assessment of cerebral blood flow in Alzheimer’s disease by spin-labeled magnetic resonance imaging, Ann Neurol47, 93–100.
23.
KanetaT, KatsuseO, HiranoT, OgawaM, Shihikura-HinoA, YoshidaK, OdawaraT, HirayasuY, InoueT (2017) Voxel-wise correlations between cognition and cerebral blood flow using arterial spin-labeled perfusion MRI in patients with Alzheimer’s disease: A cross-sectional study, BMC Neurol17, 91.
24.
BinnewijzendMA, BenedictusMR, KuijerJP, van der FlierWM, TeunissenCE, PrinsND, WattjesMP, van BerckelBN, ScheltensP, BarkhofF (2016) Cerebral perfusion in the predementia stages of Alzheimer’s disease, Eur Radiol26, 506–514.
25.
BenedictusMR, LeeuwisAE, BinnewijzendMA, KuijerJP, ScheltensP, BarkhofF, van der FlierWM, PrinsND (2017) Lower cerebral blood flow is associated with faster cognitive decline in Alzheimer’s disease, Eur Radiol27, 1169–1175.
26.
LehmannM, MelbourneA, DicksonJC, AhmedRM, ModatM, CardosoMJ, ThomasDL, De VitaE, CrutchSJ, WarrenJD, MahoneyCJ, BomanjiJ, HuttonBF, FoxNC, GolayX, OurselinS, SchottJM (2016) A novel use of arterial spin labelling MRI to demonstrate focal hypoperfusion in individuals with posterior cortical atrophy: A multimodal imaging study, J Neurol Neurosurg Psychiatry87, 1032–1034.
27.
MattssonN, TosunD, InselPS, SimonsonA, JackCRJr., BeckettLA, DonohueM, JagustW, SchuffN, WeinerMW (2014) Association of brain amyloid-β with cerebral perfusion and structure in Alzheimer’s disease and mild cognitive impairment, Brain137, 1550–1561.
28.
VerclytteS, LopesR, LenfantP, RollinA, SemahF, LeclercX, PasquierF, DelmaireC (2016) Cerebral hypoperfusion and hypometabolism detected by arterial spin labeling MRI and FDG-PET in early-onset Alzheimer’s disease, J Neuroimaging26, 207–212.
29.
MaoC, LiJ, HuangX, DongL, LiuC, PengB, CuiL, GaoJ (2021) White matter hyperintensities and patterns of atrophy in early onset Alzheimer’s disease with causative gene mutations, Clin Neurol Neurosurg203, 106552.
30.
VerclytteS, LopesR, ViardR, RollinA, VanhoutteM, PasquierF, PruvoJP, LeclercX (2020) Differences in cortical perfusion detected by arterial spin labeling in nonamnestic and amnestic subtypes of early-onset Alzheimer’s disease, J Neuroradiol47, 284–291.
31.
DoluiS, LiZ, NasrallahIM, DetreJA, WolkDA (2020) Arterial spin labeling versus (18)F-FDG-PET to identify mild cognitive impairment, Neuroimage Clin25, 102146.
32.
JohnsonNA, JahngGH, WeinerMW, MillerBL, ChuiHC, JagustWJ, Gorno-TempiniML, SchuffN (2005) Pattern of cerebral hypoperfusion in Alzheimer disease and mild cognitive impairment measured with arterial spin-labeling MR imaging: Initial experience, Radiology234, 851–859.
DingB, LingHW, ZhangY, HuangJ, ZhangH, WangT, YanFH (2014) Pattern of cerebral hyperperfusion in Alzheimer’s disease and amnestic mild cognitive impairment using voxel-based analysis of 3D arterial spin-labeling imaging: Initial experience, Clin Interv Aging9, 493–500.
35.
CamargoA, WangZ (2021) Longitudinal cerebral blood flow changes in normal aging and the Alzheimer’s disease continuum identified by arterial spin labeling MRI, J Alzheimers Dis81, 1727–1735.
36.
ChaoLL, BuckleyST, KornakJ, SchuffN, MadisonC, YaffeK, MillerBL, KramerJH, WeinerMW (2010) ASL perfusion MRI predicts cognitive decline and conversion from MCI to dementia, Alzheimer Dis Assoc Disord24, 19–27.
37.
HuWT, WangZ, LeeVM, TrojanowskiJQ, DetreJA, GrossmanM (2010) Distinct cerebral perfusion patterns in FTLD and AD, Neurology75, 881–888.
38.
SteketeeRM, BronEE, MeijboomR, HoustonGC, KleinS, MutsaertsHJ, Mendez OrellanaCP, de JongFJ, van SwietenJC, van der LugtA, SmitsM (2016) Early-stage differentiation between presenile Alzheimer’s disease and frontotemporal dementia using arterial spin labeling MRI, Eur Radiol26, 244–253.
39.
ShimizuS, ZhangY, LaxamanaJ, MillerBL, KramerJH, WeinerMW, SchuffN (2010) Concordance and discordance between brain perfusion and atrophy in frontotemporal dementia, Brain Imaging Behav4, 46–54.
40.
BronEE, SmitsM, PapmaJM, SteketeeRME, MeijboomR, de GrootM, van SwietenJC, NiessenWJ, KleinS (2017) Multiparametric computer-aided differential diagnosis of Alzheimer’s disease and frontotemporal dementia using structural and advanced MRI, Eur Radiol27, 3372–3382.
