Share:
Share this content in WeChat
X
Review
Advances in MRI of the glymphatic system in brain tumors
LIANG Xue  ZHANG Xin  ZHANG Bing 

Cite this article as: LIANG X, ZHANG X, ZHANG B. Advances in MRI of the glymphatic system in brain tumors[J]. Chin J Magn Reson Imaging, 2024, 15(12): 206-211. DOI:10.12015/issn.1674-8034.2024.12.032.


[Abstract] The glymphatic system (GS), a pivotal mechanism for waste clearance in the central nervous system, has emerged as a significant discovery in the realm of neuroscience in recent years. Advancements in MRI technology have enabled the non-invasive observation and investigation of GS's structure and function in vivo. While the dysfunction of the GS has been related to a myriad of neurological conditions, particularly within the spectrum of neurodegenerative diseases, its role in the context of brain tumors has been less extensively explored. This review comprehensively summarizes the anatomy and physiology of the GS, identifies factors that can damage it, and introduces principal MRI-based assessment methods. It explores the role of the GS in the pathological changes associated with brain tumors and discusses its potential applications in the diagnosis and treatment of these tumors, aiming to provide novel perspectives and methodologies for research in this field.
[Keywords] glymphatic system;magnetic resonance imaging;brain tumors;therapy;pathophysiology

LIANG Xue1, 2   ZHANG Xin2   ZHANG Bing1, 2*  

1 Department of Radiology, Nanjing Drum Tower Hospital Clinical College of Nanjing Medical University, Nanjing210008, China

2 Department of Radiology, the Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing210008, China

Corresponding author: ZHANG B, E-mail: zhangbing_nanjing@nju.edu.cn

Conflicts of interest   None.

Received  2024-08-09
Accepted  2024-12-10
DOI: 10.12015/issn.1674-8034.2024.12.032
Cite this article as: LIANG X, ZHANG X, ZHANG B. Advances in MRI of the glymphatic system in brain tumors[J]. Chin J Magn Reson Imaging, 2024, 15(12): 206-211. DOI:10.12015/issn.1674-8034.2024.12.032.

[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 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC3551275/. DOI: 10.1126/scitranslmed.3003748.
[2]
LOUVEAU A, SMIRNOV I, KEYES T J, et al. Structural and functional features of central nervous system lymphatic vessels[J]. Nature, 2015, 523(7560): 337-341. DOI: 10.1038/nature14432.
[3]
SALEHPOUR F, KHADEMI M, BRAGIN D E, et al. Photobiomodulation therapy and the glymphatic system: Promising applications for augmenting the brain lymphatic drainage system[J/OL]. Int J Mol Sci, 2022, 23(6): 2975 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC8950470/. DOI: 10.3390/ijms23062975.
[4]
WRIGHT A M, WU Y C, FENG L, et al. Diffusion magnetic resonance imaging of cerebrospinal fluid dynamics: Current techniques and future advancements[J/OL]. NMR Biomed, 2024, 37(9): e5162 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC11303114/. DOI: 10.1002/nbm.5162.
[5]
SCALIA G, FERINI G, SILVEN M P, et al. Alterations of the glymphatic system in glioblastomas: A systematic review[J]. Anticancer Res, 2024, 44(8): 3223-3230. DOI: 10.21873/anticanres.17140.
[6]
JIA Y, XU S, HAN G, et al. Transmembrane water-efflux rate measured by magnetic resonance imaging as a biomarker of the expression of aquaporin-4 in gliomas[J]. Nat Biomed Eng, 2022, 7(3): 236-252. DOI: 10.1038/s41551-022-00960-9.
[7]
LAN Y L, WANG H, CHEN A, et al. Update on the current knowledge of lymphatic drainage system and its emerging roles in glioma management[J]. Immunology, 2023, 168(2): 233-247. DOI: 10.1111/imm.13517.
[8]
LI Y, DI C, SONG S, et al. Choroid plexus mast cells drive tumor-associated hydrocephalus[J/OL]. Cell, 2023, 186(26): 5719-5738.e5728 [2024-08-09]. https://pubmed.ncbi.nlm.nih.gov/38056463/ DOI: 10.1016/j.cell.2023.11.001.
[9]
COZZI F M, AMPIE L, LAWS M T, et al. The role of the dura mater in cerebral metastases[J/OL]. Neurosurg Focus, 2023, 55(2): E17 [2024-08-09]. https://pubmed.ncbi.nlm.nih.gov/37527680/. DOI: 10.3171/2023.5.FOCUS23229.
[10]
TAOKA T, NAGANAWA S. Glymphatic imaging using MRI[J]. J Magn Reson Imaging, 2020, 51(1): 11-24. DOI: 10.1002/jmri.26892.
[11]
ILIFF J J, LEE H, YU M, et al. Brain-wide pathway for waste clearance captured by contrast-enhanced MRI[J]. J Clin Invest, 2013, 123(3): 1299-1309. DOI: 10.1172/jci67677.
[12]
XUE Y, LIU X, KOUNDAL S, et al. In vivo T1 mapping for quantifying glymphatic system transport and cervical lymph node drainage[J/OL]. Sci Rep, 2020, 10(1): 14592 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC7471332/. DOI: 10.1038/s41598-020-71582-x.
[13]
JIANG X Y, SU Y Y, HU C H, et al. Relationship between CSF inflow into the cerebral glymphatic system of AD mice and age: A visualization study based on 9.4 T DCE-MRI[J]. Chin J Magn Reson Imaging, 2024, 15(4): 113-119. DOI: 10.12015/issn.1674-8034.2024.04.018.
[14]
EIDE P K, RINGSTAD G. MRI with intrathecal MRI gadolinium contrast medium administration: a possible method to assess glymphatic function in human brain[J/OL]. Acta Radiol Open, 2015, 4(11): 2058460115609635 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC4652208/. DOI: 10.1177/2058460115609635.
[15]
RINGSTAD G, VATNEHOL S A S, EIDE P K. Glymphatic MRI in idiopathic normal pressure hydrocephalus[J]. Brain, 2017, 140(10): 2691-2705. DOI: 10.1093/brain/awx191.
[16]
KAUR J, DING G, ZHANG L, et al. Imaging glymphatic response to glioblastoma[J/OL]. Cancer Imaging, 2023, 23(1): 107 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC10614361/. DOI: 10.1186/s40644-023-00628-w.
[17]
XU D, ZHOU J, MEI H, et al. Impediment of cerebrospinal fluid drainage through glymphatic system in glioma[J/OL]. Front Oncol, 2021, 11: 790821 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC8784869/. DOI: 10.3389/fonc.2021.790821.
[18]
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.
[19]
TOH C H, SIOW T Y. Factors associated with dysfunction of glymphatic system in patients with glioma[J/OL]. Front Oncol, 2021, 11: 744318 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC8496738/. DOI: 10.3389/fonc.2021.744318.
[20]
TOH C H, SIOW T Y, CASTILLO M. Peritumoral brain edema in metastases may be related to glymphatic dysfunction[J/OL]. Front Oncol, 2021, 11: 725354 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC8548359/. DOI: 10.3389/fonc.2021.725354.
[21]
TOH C H, SIOW T Y, CASTILLO M. Peritumoral brain edema in meningiomas may be related to glymphatic dysfunction[J/OL]. Front Neurosci, 2021, 15: 674898 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC8100232/. DOI: 10.3389/fnins.2021.674898.
[22]
TURKIN A M, MELNIKOVA-PITSKHELAURI T V, FADEEVA L M, et al. Perifocal edema and glymphatic system dysfunction: quantitative assessment based on diffusion tensor magnetic resonance imaging[J]. Zh Vopr Neirokhir Im N N Burdenko, 2023, 87(5): 45-54. DOI: 10.17116/neiro20238705145.
[23]
VILLACIS G, SCHMIDT A, RUDOLF J C, et al. Evaluating the glymphatic system via magnetic resonance diffusion tensor imaging along the perivascular spaces in brain tumor patients[J]. Jpn J Radiol, 2024, 42(10): 1146-1156. DOI: 10.1007/s11604-024-01602-7.
[24]
HALLER S, MOY L, ANZAI Y. Evaluation of diffusion tensor imaging analysis along the perivascular space as a marker of the glymphatic system[J/OL]. Radiology, 2024, 310(1): e232899 [2024-08-09]. https://pubmed.ncbi.nlm.nih.gov/38289215/. DOI: 10.1148/radiol.232899.
[25]
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.
[26]
TAOKA T, ITO R, NAKAMICHI R, et al. Evaluation of alterations in interstitial fluid dynamics in cases of whole-brain radiation using the diffusion-weighted image analysis along the perivascular space method[J/OL]. NMR Biomed, 2024, 37(7): e5030 [2024-08-09]. https://pubmed.ncbi.nlm.nih.gov/37675787/. DOI: 10.1002/nbm.5030.
[27]
ABSINTA M, HA S K, NAIR G, et al. Human and nonhuman primate meninges harbor lymphatic vessels that can be visualized noninvasively by MRI[J/OL]. eLife, 2017, 6: e29738 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC5626482/. DOI: 10.7554/eLife.29738.
[28]
DING X B, WANG X X, XIA D H, et al. Impaired meningeal lymphatic drainage in patients with idiopathic Parkinson's disease[J]. Nat Med, 2021, 27(3): 411-418. DOI: 10.1038/s41591-020-01198-1.
[29]
WANG X, TIAN H, LIU H, et al. Impaired meningeal lymphatic flow in NMOSD patients with acute attack[J/OL]. Front Immunol, 2021, 12: 692051 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC8236891/. DOI: 10.3389/fimmu.2021.692051.
[30]
POTTER G M, CHAPPELL F M, MORRIS Z, et al. Cerebral perivascular spaces visible on magnetic resonance imaging: development of a qualitative rating scale and its observer reliability[J]. Cerebrovascular diseases (Basel, Switzerland), 2015, 39(3-4): 224-231. DOI: 10.1159/000375153.
[31]
MOSES J, SINCLAIR B, LAW M, et al. Automated methods for detecting and quantitation of enlarged perivascular spaces on MRI[J]. J Magn Reson Imaging, 2022, 57(1): 11-24. DOI: 10.1002/jmri.28369.
[32]
CAI K, TAIN R, DAS S, et al. The feasibility of quantitative MRI of perivascular spaces at 7 T[J]. J Neurosci Methods, 2015, 256: 151-156. DOI: 10.1016/j.jneumeth.2015.09.001.
[33]
DEIKE K, DECKER A, SCHEYHING P, et al. Machine learning–based perivascular space volumetry in Alzheimer disease[J]. Invest Radiol, 2024, 59(9): 667-676. DOI: 10.1097/rli.0000000000001077.
[34]
MORTAZAVI M M, GRIESSENAUER C J, ADEEB N, et al. The choroid plexus: a comprehensive review of its history, anatomy, function, histology, embryology, and surgical considerations[J]. Childs Nerv Syst, 2014, 30(2): 205-214. DOI: 10.1007/s00381-013-2326-y.
[35]
SUN A, WANG J. Choroid plexus and drug removal mechanisms[J/OL]. AAPS J, 2021, 23(3): 61 [2024-08-09]. https://pubmed.ncbi.nlm.nih.gov/33942198/. DOI: 10.1208/s12248-021-00587-9.
[36]
EIDE P K, VALNES L M, PRIPP A H, et al. Delayed clearance of cerebrospinal fluid tracer from choroid plexus in idiopathic normal pressure hydrocephalus[J]. J Cereb Blood Flow Metab, 2020, 40(9): 1849-1858. DOI: 10.1177/0271678x19874790.
[37]
CHOI J D, MOON Y, KIM H J, et al. Choroid plexus volume and permeability at brain MRI within the Alzheimer disease clinical spectrum[J]. Radiology, 2022, 304(3): 635-645. DOI: 10.1148/radiol.212400.
[38]
CHRISTENSEN J, LI C, MYCHASIUK R. Choroid plexus function in neurological homeostasis and disorders: The awakening of the circadian clocks and orexins[J]. J Cereb Blood Flow Metab, 2022, 42(7): 1163-1175. DOI: 10.1177/0271678X221082786.
[39]
FOKKINGA E, HERNANDEZ-TAMAMES J A, IANUS A, et al. Advanced diffusion-weighted MRI for cancer microstructure assessment in body imaging, and its relationship with histology[J]. J Magn Reson Imaging, 2024, 60(4):1278-1304. DOI: 10.1002/jmri.29144.
[40]
CHEN L, HUANG L, ZHANG J, et al. Amide proton transfer-weighted and arterial spin labeling imaging may improve differentiation between high-grade glioma recurrence and radiation-induced brain injury[J/OL]. Heliyon, 2024, 10(11): e32699 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC11219995/ DOI: 10.1016/j.heliyon.2024.e32699.
[41]
JABEHDAR MARALANI P, CHAN R W, LAM W W, et al. Chemical exchange saturation transfer MRI: What neuro-oncology clinicians need to know[J/OL]. Technol Cancer Res Treat, 2023, 22: 15330338231208613 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC10594966/. DOI: 10.1177/15330338231208613.
[42]
KAMAGATA K, ANDICA C, TAKABAYASHI K, et al. Association of MRI indices of glymphatic system with amyloid deposition and cognition in mild cognitive impairment and Alzheimer disease[J/OL]. Neurology, 2022, 99(24): e2648-e2660 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC9757870/. DOI: 10.1212/wnl.0000000000201300.
[43]
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 [2024-08-09]. https://pmc.ncbi.nlm.nih.gov/articles/PMC9772196/. DOI: 10.1038/s41531-022-00437-1.
[44]
GAO M, LIU Z, ZANG H, et al. A histopathologic correlation study evaluating glymphatic function in brain tumors by multi-parametric MRI[J]. Clin Cancer Res, 2024, 30(21): 4876-4886. DOI: 10.1158/1078-0432.
[45]
SHANG P, ZHENG R, WU K, et al. New insights on mechanisms and therapeutic targets of cerebral edema[J]. Curr Neuropharmacol, 2024, 22(14): 2330-2352. DOI: 10.2174/1570159x22666240528160237.

PREV Advances in the application of 7 T magnetic resonance imaging in brain tumor diagnosis
NEXT Research progress of multimodal imaging techniques in high myopia
  



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