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• Clinical Article •
Value of DTI combined with ASL imaging in evaluating the cognitive impairment of asymptomatic Moyamoya disease in adults
FU Lin  QIN Yuanlin  LI Xin  NIU Ruoxin  YUAN Xuexia  LIU Deguo 

DOI:10.12015/issn.1674-8034.2026.02.004.


[Abstract] Objective To explore the application value of diffusion tensor imaging (DTI) combined with arterial spin labeling (ASL) in cognitive impairment (CI) of asymptomatic Moyamoya disease (MMD) in adults.Materials and Methods DTI and ASL were performed in 81 patients with MMD (40 patients with MMD-CI and 41 patients with MMD-NCI) and 43 healthy controls (HC). The differences and correlations of DTI and ASL parameters in different brain regions of each group were compared and analyzed.Results Compared with MMD-NCI group and HC group, the apparent diffusion coefficient (ADC) of white matter, corpus callosum, right semi-oval center and left cingulate gyrus in bilateral frontal subcortex, corona radiata, anterior horn of lateral ventricle and trigone of lateral ventricle in MMD-CI group increased (P < 0.05), the fractional anisotropy (FA) of bilateral frontal subcortex, corona radiata, corpus callosum and right anterior horn of lateral ventricle decreased (P < 0.05), and the cerebral blood flow (CBF) of bilateral semi-oval center, corona radiata, right frontal subcortex and right cingulate gyrus decreased (P < 0.05). The ADC values of left corona radiata, corpus callosum, right anterior horn of ventricle, left anterior horn of ventricle and right trigone of ventricle were negatively correlated with CBF values (r = -0.47, -0.44, -0.38, -0.27, -0.26). The FA values of left corona radiata, corpus callosum, right anterior horn of ventricle, left trigone of ventricle and right hippocampal head were positively correlated with CBF values (r = 0.44, 0.42, 0.39, 0.37, 0.33). The FA values of double corona radiata, corpus callosum, left frontal subcortical and right ventricular anterior horn in MMD-CI group were lower than those in MMD-NCI group, and the differences were statistically significant (P < 0.05).Conclusions DTI and ASL can reveal the abnormal changes of white matter in adult MMD patients. FA value may be a sensitive imaging index to identify cognitive impairment in adult MMD patients.
[Keywords] asymptomatic Moyamoya disease in adults；cognitive impairment；magnetic resonance imaging；diffusion tensor imaging；arterial spin labeling

FU Lin1, 2   QIN Yuanlin1   LI Xin3   NIU Ruoxin3   YUAN Xuexia1   LIU Deguo1*  

1 Department of Medical Imaging, Affiliated Hospital of Jining Medical University, Jining 272029, China

2 Imaging Center of Tengzhou Central People's Hospital, Zaozhuang 277599, China

3 Clinical School, Jining Medical University, Jining 272013, China

Corresponding author: LIU D G, E-mail: sdjnliudeguo@163.com

Conflicts of interest   None.

Received  2025-10-13
Accepted  2025-12-29
DOI: 10.12015/issn.1674-8034.2026.02.004
DOI:10.12015/issn.1674-8034.2026.02.004.

[1]
FUJIMURA M, TOMINAGA T, KURODA S, et al. 2021 Japanese Guidelines for the Management of Moyamoya Disease: Guidelines from the Research Committee on Moyamoya Disease and Japan Stroke Society[J]. Neurol Med Chir (Tokyo), 2022, 62(4): 165-170. DOI: 10.2176/jns-nmc.2021-0382.
[2]
Neurosurgical Branch of Chinese Medical Association. Chinese expert consensus on the diagnosis and treatment of Moyamoya disease and Moyamoya syndrome (2024 edition)[J]. Chin J Neurosurg, 2024, 40(3): 220-229. DOI: 10.3760/cma.j.cn112050-20231119-00177.
[3]
LI J, LIU X, ZHANG D, et al. Cognitive Performance Profile in Pediatric Moyamoya Disease Patients and Its Relationship With Regional Cerebral Blood Perfusion[J/OL]. Front Neurol, 2019, 10: 1308 [2025-10-13]. https://doi.org/10.3389/fneur.2019.01308. DOI: 10.3389/fneur.2019.01308.
[4]
GIROUD M, CALVIERE L, MACHADO C, et al. Prevalence and characteristics of vascular cognitive impairment in a European cohort of adult patients with Moyamoya angiopathy[J]. J Neurol, 2024, 271(9): 5976-5984. DOI: 10.1007/s00415-024-12555-2.
[5]
SHEN X X, ZHANG H D, XU J L, et al. Assessment of psychological and cognitive funetion and influencing factors of cognitive function in adult patients with Moyamoya disease[J]. Chinese Journal of Cerebrovascular Diseases, 2022, 19(4): 254-263. DOI: 10.3969/j.issn.1672-5921.2022.04.006.
[6]
SHI Z, WEN Y J, HUANG Z, et al. Different aspects of cognitive function in adult patients with Moyamoya disease and its clinical subtypes[J]. Stroke Vasc Neurol, 2020, 5(1): 86-96. DOI: 10.1136/svn-2019-000309.
[7]
FU L, YU H, LIU D G. Advances in functional magnetic resonance imaging in cognitive impairment of Moyamoya disease[J]. Chin J Magn Reson Imaging, 2024, 15(1): 189-193. DOI: 10.12015/issn.1674-8034.2024.01.032.
[8]
KRONENBURG A, VAN DEN BERG E, VAN SCHOONEVELD M M, et al. Cognitive Functions in Children and Adults with Moyamoya Vasculopathy: A Systematic Review and Meta-Analysis[J]. J Stroke, 2018, 20(3): 332-341. DOI: 10.5853/jos.2018.01550.
[9]
WANG X, LIU Z, ZHOU Z, et al. Cognitive dysfunction in Moyamoya disease: latest developments and future directions[J/OL]. Front Hum Neurosci, 2024, 18: 1502318 [2025-10-13]. https://doi.org/10.3389/fnhum.2024.1502318. DOI: 10.3389/fnhum.2024.1502318.
[10]
CHAN E, GAL A M, VAN HARSKAMP N, et al. Long-term study of the cognitive profile of Moyamoya Disease in adults [J/OL]. J Stroke Cerebrovasc Dis, 2023, 32(6): 107064 [2025-10-13]. https://doi.org/10.1016/j.jstrokecerebrovasdis.2023.107064. DOI: 10.1016/j.jstrokecerebrovasdis.2023.107064.
[11]
MAEHARA N, NAKAMIZO A, ARIMURA K, et al. Memory, Executive, and Intellectual Functions in Adults with Moyamoya Disease[J/OL]. World Neurosurg, 2023, 180: e474-e83 [2025-10-13]. https://doi.org/10.1016/j.wneu.2023.09.092. DOI: 10.1016/j.wneu.2023.09.092.
[12]
HE S, LIU Z, WEI Y, et al. Impairments in brain perfusion, executive control network, topological characteristics, and neurocognition in adult patients with asymptomatic Moyamoya disease[J/OL]. BMC Neurosci, 2021, 22(1): 35 [2025-10-13]. https://doi.org/10.1186/s12868-021-00638-z. DOI: 10.1186/s12868-021-00638-z.
[13]
HAO X, LIU Z, HE S, et al. Application of DTI and fMRI in Moyamoya disease[J/OL]. Front Neurol, 2022, 13: 948830 [2025-10-13]. https://doi.org/10.3389/fneur.2022.948830. DOI: 10.3389/fneur.2022.948830.
[14]
LI J, MENG Q, HUANG L, et al. Pseudo-continuous and territorial arterial spin labeling MRI for assessment of cerebral perfusion in Moyamoya disease after revascularization: A comparative study with digital subtraction angiography[J/OL]. Heliyon, 2024, 10(17): e37368 [2025-10-13]. https://doi.org/10.1016/j.heliyon.2024.e37368. DOI: 10.1016/j.heliyon.2024.e37368.
[15]
KARZMARK P, ZEIFERT P D, BELL-STEPHENS T E, et al. Neurocognitive impairment in adults with Moyamoya disease without stroke[J]. Neurosurgery, 2012, 70(3): 634-638. DOI: 10.1227/NEU.0b013e3182320d1a.
[16]
JO K I, YEON J Y, HONG S C, et al. Clinical Course of Asymptomatic Adult Moyamoya Disease[J]. Cerebrovascular Diseases, 2014, 37(2): 94-101. DOI: 10.1159/000356350.
[17]
KHAW J, SUBRAMANIAM P, AZIZ N A ABD, et al. Current Update on the Clinical Utility of MMSE and MoCA for Stroke Patients in Asia: A Systematic Review[J/OL]. Int J Environ Res Public Health, 2021, 18(17): 8962 [2025-10-13]. https://doi.org/10.3390/ijerph18178962. DOI: 10.3390/ijerph18178962.
[18]
LI H, JIA J, YANG Z. Mini-Mental State Examination in Elderly Chinese: A Population-Based Normative Study[J]. J Alzheimers Dis, 2016, 53(2): 487-496. DOI: 10.3233/JAD-160119.
[19]
LIU Z, HE S, XU Z, et al. Association between white matter impairment and cognitive dysfunction in patients with ischemic Moyamoya disease[J/OL]. BMC Neurol, 2020, 20(1): 302 [2023-10-13]. https://doi.org/10.1186/s12883-020-01876-0. DOI: 10.1186/s12883-020-01876-0.
[20]
ZHU H, ZHU C, LIU T, et al. Alterations in the Glymphatic System and Association with Brain Structure and Cognitive Function in Moyamoya Disease[J]. Transl Stroke Res, 2024, 16(4): 1173-1184. DOI: 10.1007/s12975-024-01296-z.
[21]
SHEN X X, ZHANG H D, FU H G, et al. Association of cognitive function and hypoperfusion in Moyamoya disease patients without stroke[J]. J Cereb Blood Flow Metab, 2023, 43(4): 542-551. DOI: 10.1177/0271678X221140349.
[22]
SU J B, XI S D, ZHOU S Y, et al. Microstructural damage pattern of vascular cognitive impairment: a comparison between Moyamoya disease and cerebrovascular atherosclerotic disease[J]. Neural Regen Res, 2019, 14(5): 858-867. DOI: 10.4103/1673-5374.249234.
[23]
ZHENG W, QIN X, MU R, et al. Prediction models for cognitive impairment in middle-aged patients with cerebral small vessel disease[J/OL]. Front Neurol, 2025, 16: 1462636 [2025-10-13]. https://doi.org/10.3389/fneur.2025.1462636. DOI: 10.3389/fneur.2025.1462636.
[24]
HUANG H, ZHAO K, ZHU W, et al. Abnormal Cerebral Blood Flow and Functional Connectivity Strength in Subjects With White Matter Hyperintensities[J/OL]. Front Neurol, 2021, 12: 752762 [2025-10-13]. https://doi.org/10.3389/fneur.2021.752762. DOI: 10.3389/fneur.2021.752762.
[25]
TAE W S, HAM B J, PYUN S B, et al. Current Clinical Applications of Diffusion-Tensor Imaging in Neurological Disorders[J]. J Clin Neurol, 2018, 14(2): 129-140. DOI: 10.3988/jcn.2018.14.2.129.
[26]
GIROUD M, PLANTON M, DARCOURT J, et al. MRI hypoperfusion as a determinant of cognitive impairment in adults with Moyamoya angiopathy[J]. Eur Stroke J, 2024, 9(3): 732-742. DOI: 10.1177/23969873241240829.
[27]
LOPE-PIEDRAFITA S. Diffusion Tensor Imaging (DTI)[J]. Methods Mol Biol, 2018, 1718: 103-116. DOI: 10.1007/978-1-4939-7531-0_7.
[28]
LI X T, WANG K, AI L. Preliminary study of diffusion tensor imaging and 18F-AV1451 PET tau protein brain imaging in the diagnosis and differential diagnosis of MCI[J]. Chin J Magn Reson Imaging, 2022, 13(4): 5-14. DOI: 10.12015/issn.1674-8034.2022.04.002.
[29]
KAZUMATA K, THA K K, TOKAIRIN K, et al. Brain Structure, Connectivity, and Cognitive Changes Following Revascularization Surgery in Adult Moyamoya Disease[J/OL]. Neurosurgery, 2019, 85(5): E943-E952 [2025-10-13]. https://doi.org/10.1093/neuros/nyz176. DOI: 10.1093/neuros/nyz176.
[30]
KAZUMATA K, TOKAIRIN K, ITO M, et al. Combined structural and diffusion tensor imaging detection of ischemic injury in Moyamoya disease: relation to disease advancement and cerebral hypoperfusion[J]. J Neurosurg, 2020, 134(3): 1155-1164. DOI: 10.3171/2020.1.JNS193260.
[31]
CHEN Y, WANG Y, SONG Z, et al. Abnormal white matter changes in Alzheimer's disease based on diffusion tensor imaging: A systematic review[J/OL]. Ageing Res Rev, 2023, 87: 101911 [2025-10-13]. https://doi.org/10.1016/j.arr.2023.101911. DOI: 10.1016/j.arr.2023.101911.
[32]
KAZUMATA K, THA K K, NARITA H, et al. Chronic ischemia alters brain microstructural integrity and cognitive performance in adult Moyamoya disease[J]. Stroke, 2015, 46(2): 354-360. DOI: 10.1161/STROKEAHA.114.007407.
[33]
HU J, LI Y, TONG Y, et al. Moyamoya Disease With Initial Ischemic or Hemorrhagic Attack Shows Different Brain Structural and Functional Features: A Pilot Study[J/OL]. Front Neurol, 2022, 13: 871421 [2023-10-13]. https://doi.org/10.3389/fneur.2022.871421. DOI: 10.3389/fneur.2022.871421.
[34]
CALVIERE L, CATALAA I, MARLATS F, et al. Correlation between cognitive impairment and cerebral hemodynamic disturbances on perfusion magnetic resonance imaging in European adults with Moyamoya disease. Clinical article[J]. J Neurosurg, 2010, 113(4): 753-759. DOI: 10.3171/2010.4.JNS091808.
[35]
LI W P, WANG F F, ZHANG X, et al. Study on age and white matter neuronal integrity in healthy volunteers based on automating fiber-tract quantification[J]. Natl Med J China, 2017, 97(13): 976-981. DOI: 10.3760/cma.j.issn.0376-2491.2017.13.003.
[36]
KATO D, AOYAMA Y, NISHIDA K, et al. Regulation of lipid synthesis in myelin modulates neural activity and is required for motor learning[J]. Glia, 2023, 71(11): 2591-2608. DOI: 10.1002/glia.24441.
[37]
DOLUI S, TISDALL D, VIDORRETA M, et al. Characterizing a perfusion-based periventricular small vessel region of interest[J/OL]. Neuroimage Clin, 2019, 23: 101897 [2025-10-13]. https://doi.org/10.1016/j.nicl.2019.101897. DOI: 10.1016/j.nicl.2019.101897.
[38]
MARTIN-NOGUEROL T, KIRSCH C F E, MONTESINOS P, et al. Arterial spin labeling for head and neck lesion assessment: technical adjustments and clinical applications[J]. Neuroradiology, 2021, 63(12): 1969-1983. DOI: 10.1007/s00234-021-02772-1.
[39]
HARA S, TANAKA Y, UEDA Y, et al. Noninvasive Evaluation of CBF and Perfusion Delay of Moyamoya Disease Using Arterial Spin-Labeling MRI with Multiple Postlabeling Delays: Comparison with 15O-Gas PET and DSC-MRI[J]. AJNR Am J Neuroradiol, 2017, 38(4): 696-702. DOI: 10.3174/ajnr.A5068.
[40]
XU M L, LI L J. Research progress of cognitive impairment associated with Moyamoya disease in adults[J]. Chinese Journal of Cerebrovascular Diseases, 2025, 22(4): 256-263. DOI: 10.3969/j.issn.1672-5921.2025.04.005.
[41]
HARA S, HORI M, UEDA R, et al. Unraveling Specific Brain Microstructural Damage in Moyamoya Disease Using Diffusion Magnetic Resonance Imaging and Positron Emission Tomography[J]. J Stroke Cerebrovasc Dis, 2019, 28(4): 1113-1125. DOI: 10.1016/j.jstrokecerebrovasdis.2018.12.038.
[42]
FERRIS J K, GREELEY B, VAVASOUR I M, et al. In vivo myelin imaging and tissue microstructure in white matter hyperintensities and perilesional white matter[J/OL]. Brain Commun, 2022, 4(3): fcac142 [2025-10-13]. https://doi.org/10.1093/braincomms/fcac142. DOI: 10.1093/braincomms/fcac142.
[43]
HUANG H T, TUNG T H, LIN M, et al. Characterizing spatiotemporal progression and prediction of infarct lesion volumes in experimental acute ischemia using quantitative perfusion and diffusion imaging[J/OL]. Appl Radiat Isot, 2021, 168: 109522 [2025-10-13]. https://doi.org/10.1016/j.apradiso.2020.109522. DOI: 10.1016/j.apradiso.2020.109522.
[44]
YU S, MA S J, LIEBESKIND D S, et al. Reperfusion Into Severely Damaged Brain Tissue Is Associated With Occurrence of Parenchymal Hemorrhage for Acute Ischemic Stroke[J/OL]. Front Neurol, 2020, 11: 586 [2025-10-13]. https://doi.org/10.3389/fneur.2020.00586. DOI: 10.3389/fneur.2020.00586.
[45]
YUAN X X, XUE X L, LI M Q, et al. Value of CT perfusion in evaluating the efficacy of different vascular reconstruction methods in the treatment of adult ischemic Moyamoya disease[J]. J Chin Physician, 2025, 27(2): 189-194. DOI: 10.3760/cma.j.cn431274-20240129-00202.

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