Share：
Share this content in WeChat
X
[Chinese][PDF]661
• Review •
Research progress on the glymphatic system of patients with central nervous system diseases based on diffusion tensor image analysis along the perivascular space
ZHU Xiaoying  ZHOU Tianyu  HUANG Qiang  MA Hongwei  ZHANG Qing 

Cite this article as: ZHU X Y, ZHOU T Y, HUANG Q, et al. Research progress on the glymphatic system of patients with central nervous system diseases based on diffusion tensor image analysis along the perivascular space[J]. Chin J Magn Reson Imaging, 2024, 15(6): 166-171. DOI:10.12015/issn.1674-8034.2024.06.026.


[Abstract] The glymphatic system (GS) is an emerging perspective in exploring the physiological and pathological mechanisms of central nervous system diseases in recent years. Research has confirmed that the diffusion tensor image analysis along the perivascular space (DTI-ALPS) method can effectively evaluate the functional changes of the GS in patients with central nervous system diseases, especially in degenerative central nervous system diseases, such as epilepsy, Parkinson's disease, and dementia. This article reviews the current research status of applying DTI-ALPS technology to evaluate GS function in patients with central nervous system diseases, aiming to provide new directions for neuroimaging research.
[Keywords] central nervous system diseases；glymphatic system；magnetic resonance imaging；diffusion tensor image analysis along the perivascular space

ZHU Xiaoying   ZHOU Tianyu   HUANG Qiang   MA Hongwei   ZHANG Qing*  

Department of Radiology, Zhongshan Hospital Affiliated to Dalian University, Dalian 116001, China

Corresponding author: ZHANG Q, E-mail: zhangqingsmile@163.com

Conflicts of interest   None.

Received  2024-01-29
Accepted  2024-05-30
DOI: 10.12015/issn.1674-8034.2024.06.026
Cite this article as: ZHU X Y, ZHOU T Y, HUANG Q, et al. Research progress on the glymphatic system of patients with central nervous system diseases based on diffusion tensor image analysis along the perivascular space[J]. Chin J Magn Reson Imaging, 2024, 15(6): 166-171. DOI:10.12015/issn.1674-8034.2024.06.026.

[1]
ILIFF J J, WANG M, LIAO Y, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β[J/OL]. Sci Transl Med, 2012, 4(147): 147ra111 [2024-01-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3551275/. DOI: 10.1126/scitranslmed.3003748.
[2]
SPECTOR R, ROBERT SNODGRASS S, JOHANSON C E. A balanced view of the cerebrospinal fluid composition and functions: Focus on adult humans[J]. Exp Neurol, 2015, 273: 57-68. DOI: 10.1016/j.expneurol.2015.07.027.
[3]
RASMUSSEN M K, MESTRE H, NEDERGAARD M. The glymphatic pathway in neurological disorders[J]. Lancet Neurol, 2018, 17(11): 1016-1024. DOI: 10.1016/S1474-4422(18)30318-1.
[4]
MEZEY É, SZALAYOVA I, HOGDEN C T, et al. An immunohistochemical study of lymphatic elements in the human brain[J/OL]. Proc Natl Acad Sci U S A, 2021, 118(3): e2002574118 [2024-01-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/33446503/. DOI: 10.1073/pnas.2002574118.
[5]
SHEN T, YUE Y, BA F, et al. Diffusion along perivascular spaces as marker for impairment of glymphatic system in Parkinson's disease[J/OL]. NPJ Parkinsons Dis, 2022, 8(1): 174 [2024-01-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9772196/. DOI: 10.1038/s41531-022-00437-1.
[6]
SHOKRI-KOJORI E, WANG G J, WIERS C E, et al. β-Amyloid accumulation in the human brain after one night of sleep deprivation[J]. Proc Natl Acad Sci U S A, 2018, 115(17): 4483-4488. DOI: 10.1073/pnas.1721694115.
[7]
BUCCELLATO F R, D'ANCA M, SERPENTE M, et al. The role of glymphatic system in Alzheimer's and Parkinson's disease pathogenesis[J/OL]. Biomedicines, 2022, 10(9): 2261 [2024-01-29]. https://www.mdpi.com/2227-9059/10/9/2261. DOI: 10.3390/biomedicines10092261.
[8]
TAOKA T, NAGANAWA S. Glymphatic imaging using MRI[J]. J Magn Reson Imaging, 2020, 51(1): 11-24. DOI: 10.1002/jmri.26892.
[9]
KIVINIEMI V, WANG X, KORHONEN V, et al. Ultra-fast magnetic resonance encephalography of physiological brain activity – Glymphatic pulsation mechanisms?[J]. J Cereb Blood Flow Metab, 2016, 36(6): 1033-1045. DOI: 10.1177/0271678X15622047.
[10]
JOO B, WON S Y, SINKUS R, et al. Viscoelastic property of the brain assessed with magnetic resonance elastography and its association with glymphatic system in neurologically normal individuals[J]. Korean J Radiol, 2023, 24(6): 564-573. DOI: 10.3348/kjr.2022.0992.
[11]
DYKE J P, XU H S, VERMA A, et al. MRI characterization of early CNS transport kinetics post intrathecal gadolinium injection: Trends of subarachnoid and parenchymal distribution in healthy volunteers[J]. Clin Imaging, 2020, 68: 1-6. DOI: 10.1016/j.clinimag.2020.04.043.
[12]
BENVENISTE H, LEE H, OZTURK B, et al. Glymphatic cerebrospinal fluid and solute transport quantified by MRI and PET imaging[J]. Neuroscience, 2021, 474: 63-79. DOI: 10.1016/j.neuroscience.2020.11.014.
[13]
TAOKA T, MASUTANI Y, KAWAI H, et al. Evaluation of glymphatic system activity with the diffusion MR technique: diffusion tensor image analysis along the perivascular space (DTI-ALPS) in Alzheimer's disease cases[J]. Jpn J Radiol, 2017, 35(4): 172-178. DOI: 10.1007/s11604-017-0617-z.
[14]
ZHANG W, ZHOU Y, WANG J, et al. Glymphatic clearance function in patients with cerebral small vessel disease[J/OL]. Neuroimage, 2021, 238: 118257 [2024-01-29]. https://linkinghub.elsevier.com/retrieve/pii/S1053-8119(21)00534-6. DOI: 10.1016/j.neuroimage.2021.118257.
[15]
LEE D A, PARK B S, KO J, et al. Glymphatic system function in patients with newly diagnosed focal epilepsy[J/OL]. Brain Behav, 2022, 12(3): e2504 [2024-01-29]. https://onlinelibrary.wiley.com/doi/10.1002/brb3.2504. DOI: 10.1002/brb3.2504.
[16]
LEE D A, PARK B S, KO J, et al. Glymphatic system dysfunction in temporal lobe epilepsy patients with hippocampal sclerosis[J]. Epilepsia Open, 2022, 7(2): 306-314. DOI: 10.1002/epi4.12594.
[17]
HAN G, ZHOU Y, ZHANG K, et al. Age- and time-of-day dependence of glymphatic function in the human brain measured via two diffusion MRI methods[J/OL]. Front Aging Neurosci, 2023, 15: 1173221 [2024-01-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/37284019/. DOI: 10.3389/fnagi.2023.1173221.
[18]
HSIAO W C, CHANG H I, HSU S W, et al. Association of cognition and brain reserve in aging and glymphatic function using diffusion tensor image-along the perivascular space (DTI-ALPS)[J]. Neuroscience, 2023, 524: 11-20. DOI: 10.1016/j.neuroscience.2023.04.004.
[19]
WANG J, ZHOU Y, ZHANG K, et al. Glymphatic function plays a protective role in ageing-related cognitive decline[J/OL]. Age Ageing, 2023, 52(7): afad107 [2024-01-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10314787/. DOI: 10.1093/ageing/afad107.
[20]
CAI X, CHEN Z, HE C, et al. Diffusion along perivascular spaces provides evidence interlinking compromised glymphatic function with aging in Parkinson's disease[J]. CNS Neurosci Ther, 2023, 29(1): 111-121. DOI: 10.1111/cns.13984.
[21]
SIOW T Y, TOH C H, HSU J L, et al. Association of sleep, neuropsychological performance, and gray matter volume with glymphatic function in community-dwelling older Adults[J/OL]. Neurology, 2022, 98(8): e829-e838 [2024-01-29]. https://pubmed.ncbi.nlm.nih.gov/34906982/. DOI: 10.1212/WNL.0000000000013215.
[22]
TAOKA T, ITO R, NAKAMICHI R, et al. Diffusion-weighted image analysis along the perivascular space (DWI-ALPS) for evaluating interstitial fluid status: age dependence in normal subjects[J]. Jpn J Radiol, 2022, 40(9): 894-902. DOI: 10.1007/s11604-022-01275-0.
[23]
QIN Y, LI X, QIAO Y, et al. DTI-ALPS: An MR biomarker for motor dysfunction in patients with subacute ischemic stroke[J/OL]. Front Neurosci, 2023, 17: 1132393 [2024-01-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10102345/. DOI: 10.3389/fnins.2023.1132393.
[24]
SOARES J M, MARQUES P, ALVES V, et al. A hitchhiker's guide to diffusion tensor imaging[J/OL]. Front Neurosci, 2013, 7: 31 [2024-05-21]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3594764/. DOI: 10.3389/fnins.2013.00031.
[25]
MA X, LI S, LI C, et al. Diffusion tensor imaging along the perivascular space index in different stages of Parkinson's disease[J/OL]. Front Aging Neurosci, 2021, 13: 773951 [2024-01-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8634754/. DOI: 10.3389/fnagi.2021.773951.
[26]
MCKNIGHT C D, TRUJILLO P, LOPEZ A M, et al. Diffusion along perivascular spaces reveals evidence supportive of glymphatic function impairment in Parkinson disease[J]. Parkinsonism Relat Disord, 2021, 89: 98-104. DOI: 10.1016/j.parkreldis.2021.06.004.
[27]
GU L, DAI S, GUO T, et al. Noninvasive neuroimaging provides evidence for deterioration of the glymphatic system in Parkinson's disease relative to essential tremor[J/OL]. Parkinsonism Relat Disord, 2023, 107: 105254 [2024-01-29]. https://linkinghub.elsevier.com/retrieve/pii/S1353-8020(22)00423-0. DOI: 10.1016/j.parkreldis.2022.105254.
[28]
RUAN X, HUANG X, LI Y, et al. Diffusion tensor imaging analysis along the perivascular space index in primary Parkinson's disease patients with and without freezing of gait[J]. Neuroscience, 2022, 506: 51-57. DOI: 10.1016/j.neuroscience.2022.10.013.
[29]
QIN Y, HE R, CHEN J, et al. Neuroimaging uncovers distinct relationships of glymphatic dysfunction and motor symptoms in Parkinson's disease[J]. J Neurol, 2023, 270(5): 2649-2658. DOI: 10.1007/s00415-023-11594-5.
[30]
SCHEFFER I E, BERKOVIC S, CAPOVILLA G, et al. ILAE classification of the epilepsies: Position paper of the ILAE commission for classification and terminology[J]. Epilepsia, 2017, 58(4): 512-521. DOI: 10.1111/epi.13709.
[31]
ZHANG C, XU K, ZHANG H, et al. Recovery of glymphatic system function in patients with temporal lobe epilepsy after surgery[J]. Eur Radiol, 2023, 33(9): 6116-6123. DOI: 10.1007/s00330-023-09588-y.
[32]
ZHAO X, ZHOU Y, LI Y, et al. The asymmetry of glymphatic system dysfunction in patients with temporal lobe epilepsy: A DTI-ALPS study[J]. J Neuroradiol, 2023, 50(6): 562-567. DOI: 10.1016/j.neurad.2023.05.009.
[33]
KIM J, LEE D A, LEE H J, et al. Glymphatic system dysfunction in patients with occipital lobe epilepsy[J]. J Neuroimaging, 2023, 33(3): 455-461. DOI: 10.1111/jon.13083.
[34]
LEE H J, LEE D A, SHIN K J, et al. Glymphatic system dysfunction in patients with juvenile myoclonic epilepsy[J]. J Neurol, 2022, 269(4): 2133-2139. DOI: 10.1007/s00415-021-10799-w.
[35]
LEE D A, LEE J, PARK K M. Glymphatic system impairment in patients with status epilepticus[J]. Neuroradiology, 2022, 64(12): 2335-2342. DOI: 10.1007/s00234-022-03018-4.
[36]
Neurology Branch of Chinese Medical Association, Cerebrovascular Disease Group of Neurology Branch of Chinese Medicial Association, Classification of cerebrovascular diseases in China (2015)[J]. Chin J Neurol, 2017, 50(3): 168-171. DOI: 10.3760/cma.j.issn.1006-7876.2017.03.003.
[37]
TOH C H, SIOW T Y. Glymphatic dysfunction in patients with ischemic stroke[J/OL]. Front Aging Neurosci, 2021, 13: 756249 [2024-01-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8606520/. DOI: 10.3389/fnagi.2021.756249.
[38]
ZHANG C, SHA J, CAI L, et al. Evaluation of the glymphatic system using the DTI-ALPS index in patients with spontaneous intracerebral haemorrhage[J]. Oxid Med Cell Longev, 2022, 2022: 1-7. DOI: 10.1155/2022/2694316.
[39]
DUERING M, BIESSELS G J, BRODTMANN A, et al. Neuroimaging standards for research into small vessel disease—advances since 2013[J]. Lancet Neurol, 2023, 22(7): 602-618. DOI: 10.1016/S1474-4422(23)00131-X.
[40]
TIAN Y, CAI X, ZHOU Y, et al. Impaired glymphatic system as evidenced by low diffusivity along perivascular spaces is associated with cerebral small vessel disease: a population-based study[J]. Stroke Vasc Neurol, 2023, 8(5): 413-423. DOI: 10.1136/svn-2022-002191.
[41]
LI Y, ZHOU Y, ZHONG W, et al. Choroid plexus enlargement exacerbates white matter hyperintensity growth through glymphatic impairment[J]. Ann Neurol, 2023, 94(1): 182-195. DOI: 10.1002/ana.26648.
[42]
GALE S A, ACAR D, DAFFNER K R. Dementia[J]. Am J Med, 2018, 131(10): 1161-1169. DOI: 10.1016/j.amjmed.2018.01.022.
[43]
HARRSION I F, ISMAIL O, MACHHADA A, et al. Impaired glymphatic function and clearance of tau in an Alzheimer's disease model[J]. Brain, 2020, 143(8): 2576-2593. DOI: 10.1093/brain/awaa179.
[44]
STEWARD C E, VENKATRAMAN V K, LUI E, et al. Assessment of the DTI-ALPS parameter along the perivascular space in older adults at risk of dementia[J]. J Neuroimaging, 2021, 31(3): 569-578. DOI: 10.1111/jon.12837.
[45]
OTA M, SATO N, NAKAYA M, et al. Relationships between the deposition of amyloid-β and tau protein and glymphatic system activity in Alzheimer's disease: Diffusion tensor image study[J]. J Alzheimers Dis, 2022, 90(1): 295-303. DOI: 10.3233/JAD-220534.
[46]
HSU J, WEI Y, TOH C H, et al. Relationships between the deposition of amyloid-β and tau protein and glymphatic system activity in Alzheimer's disease: Diffusion tensor image study[J]. Ann Neurol, 2023, 93(1): 164-174. DOI: 10.1002/ana.26516.
[47]
LIANG T, CHANG F, HUANG Z, et al. Evaluation of glymphatic system activity by diffusion tensor image analysis along the perivascular space (DTI-ALPS) in dementia patients[J/OL]. Br J Radiol, 2023, 96(1146): 20220315 [2024-01-29]. https://academic.oup.com/bjr/article-lookup/doi/10.1259/bjr.20220315. DOI: 10.1259/bjr.20220315.
[48]
JIANG D, LIU L, KONG Y, et al. Regional glymphatic abnormality in behavioral variant frontotemporal dementia[J]. Ann Neurol, 2023, 94(3): 442-456. DOI: 10.1002/ana.26710.
[49]
CHANG H, HUANG C, HSU S, et al. Gray matter reserve determines glymphatic system function in young‐onset Azheimer's disease: Evidenced by DTI‐ALPS and compared with age‐matched controls[J]. Psychiatry Clin Neurosci, 2023, 77(7): 401-409. DOI: 10.1111/pcn.13557.
[50]
BAE Y J, CHOI B S, KIM J M, et al. Altered glymphatic system in idiopathic normal pressure hydrocephalus[J]. Parkinsonism Relat Disord, 2021, 82: 56-60. DOI: 10.1016/j.parkreldis.2020.11.009.
[51]
PARK J H, BAE Y J, KIM J S, et al. Glymphatic system evaluation using diffusion tensor imaging in patients with traumatic brain injury[J]. Neuroradiology, 2023, 65(3): 551-557. DOI: 10.1007/s00234-022-03073-x.
[52]
YANG D, SUN Z, YU M, et al. Associations of MRI-derived glymphatic system impairment with global white matter damage and cognitive impairment in mild traumatic brain injury: A DTI-ALPS study[J]. J Magn Reson Imaging, 2023, 59(2): 639-647. DOI: 10.1002/jmri.28797.
[53]
KIM J, LEE D A, LEE H, et al. Glymphatic system dysfunction in patients with cluster headache[J/OL]. Brain Behav, 2022, 12(6): e2631 [2024-01-29]. https://onlinelibrary.wiley.com/doi/10.1002/brb3.2631. DOI: 10.1002/brb3.2631.
[54]
LEE D A, LEE H, PARK K M. Normal glymphatic system function in patients with migraine: A pilot study[J]. Headache, 2022, 62(6): 718-725. DOI: 10.1111/head.14320.
[55]
ROY B, NUNEZ A, AYSOLA R S, et al. Impaired glymphatic system actions in obstructive sleep apnea adults[J/OL]. Front Neurosci, 2022, 16: 884234 [2024-05-21]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9120580/. DOI: 10.3389/fnins.2022.884234.
[56]
LEE H J, LEE D A, SHIN K J, et al. Glymphatic system dysfunction in obstructive sleep apnea evidenced by DTI-ALPS[J]. Sleep Med, 2022, 89: 176-181. DOI: 10.1016/j.sleep.2021.12.013.
[57]
BAE Y J, KIM J M, CHOI B S, et al. Altered brain glymphatic flow at diffusion-tensor MRI in rapid eye movement sleep behavior disorder[J/OL]. Radiology, 2023, 307(5): e221848 [2024-05-21]. https://pubs.rsna.org/doi/10.1148/radiol.221848?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub%20%200pubmed. DOI: 10.1148/radiol.221848.
[58]
ZHENG X M, ZHANG Z, LIANG X, et al. Application of DTI-ALPS index for the analysis of the function of central glymphatic system in patients with chronic insomnia[J]. Radiol Pract, 2023, 38(12): 1508-1512. DOI: 10.13609/j.cnki.1000-0313.2023.12.003.
[59]
SUNDARAM S, HUGHES R L, PETERSON E, et al. Establishing a framework for neuropathological correlates and glymphatic system functioning in Parkinson's disease[J]. Neurosci Biobehav Rev, 2019, 103: 305-315. DOI: 10.1016/j.neubiorev.2019.05.016.
[60]
MASSEY A, BOAG M, MAGNIER A, et al. Glymphatic system dysfunction and sleep disturbance may contribute to the pathogenesis and progression of Parkinson's disease[J/OL]. Int J Mol Sci, 2022, 23(21): 12928 [2024-01-29]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9656009/. DOI: 10.3390/ijms232112928.

PREV Research progress in PET/MR for diagnosis of Alzheimer,s disease within ATN framework
NEXT Progress in MRI in peritumoral brain zone of brain tumors
  


LINK


Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn