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27-09-2023 | Parkinson's Disease | Original Communication

Correlation of glymphatic system abnormalities with Parkinson’s disease progression: a clinical study based on non-invasive fMRI

Authors: Jing-Cai Meng, Ming-Qiang Shen, Yan-Li Lu, Hong-Xuan Feng, Xin-Yi Chen, Da-Qiang Xu, Guan-Hui Wu, Qing-Zhang Cheng, Lin-Hui Wang, Qian Gui

Published in: Journal of Neurology | Issue 1/2024

Abstract

Background

The glymphatic system is reportedly involved in Parkinson’s disease (PD). Based on previous studies, we aimed to confirm the correlation between the glymphatic system and PD progression by combining two imaging parameters, diffusion tensor image analysis along the perivascular space (DTI-ALPS), and enlarged perivascular spaces (EPVS).

Methods

Fifty-one PD patients and fifty healthy control (HC) were included. Based on the Hoehn-Yahr scale, the PD group was divided into early-stage and medium-to late-stage. All PD patients were scored using the Unified PD Rating Scale (UPDRS). We assessed the DTI-ALPS indices in the bilateral hemispheres and EPVS numbers in bilateral centrum semiovale (CSO), basal ganglia (BG), and midbrain.

Results

The DTI-ALPS indices were significantly lower bilaterally in PD patients than in the HC group, and EPVS numbers in any of the bilateral CSO, BG, and midbrain were significantly higher, especially for the medium- to late-stage group and the BG region. In PD patients, the DTI-ALPS index was significantly negatively correlated with age, while the BG-EPVS numbers were significantly positively correlated with age. Furthermore, the DTI-ALPS index was negatively correlated with UPDRS II and III scores, while the BG-EPVS numbers were positively correlated with UPDRS II and III scores. Similarly, the correlation was more pronounced in the medium- to late-stage group.

Conclusion

The DTI-ALPS index and EPVS numbers (especially in the BG region) are closely related to age and PD progression and can serve as non-invasive assessments for glymphatic dysfunction and its interventions in clinical studies.

GBD (2016) Neurology Collaborators (2019) Global, regional, and national burden of neurological disorders, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 18:459–480. https://doi.org/10.1016/s1474-4422(18)30499-xCrossRef

Keir LHM, Breen DP (2020) New awakenings: current understanding of sleep dysfunction and its treatment in Parkinson’s disease. J Neurol 267:288–294. https://doi.org/10.1007/s00415-019-09651-zCrossRefPubMed

Atik A, Stewart T, Zhang J (2016) Alpha-synuclein as a biomarker for Parkinson’s disease. Brain Pathol 26:410–418. https://doi.org/10.1111/bpa.12370CrossRefPubMedPubMedCentral

Mehra S, Sahay S, Maji SK (2019) α-Synuclein misfolding and aggregation: implications in Parkinson’s disease pathogenesis. Biochim Biophys Acta Proteins Proteom 1867:890–908. https://doi.org/10.1016/j.bbapap.2019.03.001CrossRefPubMed

Tolosa E, Garrido A, Scholz SW, Poewe W (2021) Challenges in the diagnosis of Parkinson’s disease. Lancet Neurol 20:385–397. https://doi.org/10.1016/s1474-4422(21)00030-2CrossRefPubMedPubMedCentral

Reich SG, Savitt JM (2019) Parkinson’s disease. Med Clin North Am 103:337–350. https://doi.org/10.1016/j.mcna.2018.10.014CrossRefPubMed

Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen SE, N., Braak E. (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211. https://doi.org/10.1016/s0197-4580(02)00065-9CrossRefPubMed

Ugrumov M (2020) Development of early diagnosis of Parkinson’s disease: illusion or reality? CNS Neurosci Ther 26:997–1009. https://doi.org/10.1111/cns.13429CrossRefPubMedPubMedCentral

Sun BL, Wang LH, Yang T, Sun JY, Mao LL, Yang MF, Yuan H, Colvin RA, Yang XY (2018) Lymphatic drainage system of the brain: a novel target for intervention of neurological diseases. Prog Neurobiol 163–164:118–143. https://doi.org/10.1016/j.pneurobio.2017.08.007CrossRefPubMed

10.

Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med 4:147ra111. https://doi.org/10.1126/scitranslmed.3003748CrossRefPubMedPubMedCentral

11.

Aspelund A, Antila S, Proulx ST, Karlsen TV, Karaman S, Detmar M, Wiig H, Alitalo K (2015) A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J Exp Med 212:991–999. https://doi.org/10.1084/jem.20142290CrossRefPubMedPubMedCentral

12.

Da Mesquita S, Louveau A, Vaccari A, Smirnov I, Cornelison RC, Kingsmore KM, Contarino C, Onengut-Gumuscu S, Farber E, Raper D, Viar KE, Powell RD, Baker W, Dabhi N, Bai R, Cao R, Hu S, Rich SS, Munson JM, Lopes MB, Overall CC, Acton ST, Kipnis J (2018) Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease. Nature 560:185–191. https://doi.org/10.1038/s41586-018-0368-8CrossRefPubMedPubMedCentral

13.

Natale G, Limanaqi F, Busceti CL, Mastroiacovo F, Nicoletti F, Puglisi-Allegra S, Fornai F (2021) Glymphatic system as a gateway to connect neurodegeneration from periphery to CNS. Front Neurosci 15:639140. https://doi.org/10.3389/fnins.2021.639140CrossRefPubMedPubMedCentral

14.

Hablitz LM, Nedergaard M (2021) The glymphatic system. Curr Biol 31:R1371-r1375. https://doi.org/10.1016/j.cub.2021.08.026CrossRefPubMed

15.

Wang Z, Song Z, Zhou C, Fang Y, Gu L, Yang W, Gao T, Si X, Liu Y, Chen Y, Guan X, Guo T, Wu J, Bai X, Zhang M, Zhang B, Pu J (2023) Reduced coupling of global brain function and cerebrospinal fluid dynamics in Parkinson’s disease. J Cereb Blood Flow Metab. https://doi.org/10.1177/0271678x231164337CrossRefPubMedPubMedCentral

16.

Zhang Y, Zhang C, He XZ, Li ZH, Meng JC, Mao RT, Li X, Xue R, Gui Q, Zhang GX, Wang LH (2023) Interaction between the glymphatic system and α-synuclein in Parkinson’s disease. Mol Neurobiol 60:2209–2222. https://doi.org/10.1007/s12035-023-03212-2CrossRefPubMed

17.

Zou W, Pu T, Feng W, Lu M, Zheng Y, Du R, Xiao M, Hu G (2019) Blocking meningeal lymphatic drainage aggravates Parkinson’s disease-like pathology in mice overexpressing mutated α-synuclein. Transl Neurodegener 8:7. https://doi.org/10.1186/s40035-019-0147-yCrossRefPubMedPubMedCentral

18.

Harrison IF, Ismail O, Machhada A, Colgan N, Ohene Y, Nahavandi P, Ahmed Z, Fisher A, Meftah S, Murray TK, Ottersen OP, Nagelhus EA, O’Neill MJ, Wells JA, Lythgoe MF (2020) Impaired glymphatic function and clearance of tau in an Alzheimer’s disease model. Brain 143:2576–2593. https://doi.org/10.1093/brain/awaa179CrossRefPubMedPubMedCentral

19.

Rasmussen MK, Mestre H, Nedergaard M (2018) The glymphatic pathway in neurological disorders. Lancet Neurol 17:1016–1024. https://doi.org/10.1016/s1474-4422(18)30318-1CrossRefPubMedPubMedCentral

20.

Liu Y, Hu PP, Zhai S, Feng WX, Zhang R, Li Q, Marshall C, Xiao M, Wu T (2022) Aquaporin 4 deficiency eliminates the beneficial effects of voluntary exercise in a mouse model of Alzheimer’s disease. Neural Regen Res 17:2079–2088. https://doi.org/10.4103/1673-5374.335169CrossRefPubMedPubMedCentral

21.

Cui H, Wang W, Zheng X, Xia D, Liu H, Qin C, Tian H, Teng J (2021) Decreased AQP4 expression aggravates ɑ-synuclein pathology in Parkinson’s disease mice, possibly via impaired glymphatic clearance. J Mol Neurosci 71:2500–2513. https://doi.org/10.1007/s12031-021-01836-4CrossRefPubMed

22.

Ramirez-Suarez KI, Tierradentro-Garcia LO, Smith CL, Krishnamurthy G, Escobar FA, Otero HJ, Rapp JB, Dori Y, Biko DM (2022) Dynamic contrast-enhanced magnetic resonance lymphangiography. Pediatr Radiol 52:285–294. https://doi.org/10.1007/s00247-021-05051-6CrossRefPubMed

23.

Azzalini L, Candilio L, McCullough PA, Colombo A (2017) Current risk of contrast-induced acute kidney injury after coronary angiography and intervention: a reappraisal of the literature. Can J Cardiol 33:1225–1228. https://doi.org/10.1016/j.cjca.2017.07.482CrossRefPubMed

24.

Taoka T, Masutani Y, Kawai H, Nakane T, Matsuoka K, Yasuno F, Kishimoto T, Naganawa S (2017) 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. Jpn J Radiol 35:172–178. https://doi.org/10.1007/s11604-017-0617-zCrossRefPubMed

25.

Hsu JL, Wei YC, Toh CH, Hsiao IT, Lin KJ, Yen TC, Liao MF, Ro LS (2023) Magnetic resonance images implicate that glymphatic alterations mediate cognitive dysfunction in Alzheimer disease. Ann Neurol 93:164–174. https://doi.org/10.1002/ana.26516CrossRefPubMed

26.

Ota M, Sato N, Nakaya M, Shigemoto Y, Kimura Y, Chiba E, Yokoi Y, Tsukamoto T, Matsuda H (2022) Relationships between the deposition of amyloid-β and tau protein and glymphatic system activity in Alzheimer’s disease: diffusion tensor image study. J Alzheimers Dis 90:295–303. https://doi.org/10.3233/jad-220534CrossRefPubMed

27.

Cai X, Chen Z, He C, Zhang P, Nie K, Qiu Y, Wang L, Wang L, Jing P, Zhang Y (2023) Diffusion along perivascular spaces provides evidence interlinking compromised glymphatic function with aging in Parkinson’s disease. CNS Neurosci Ther 29:111–121. https://doi.org/10.1111/cns.13984CrossRefPubMed

28.

Chen X, Wang J, Shan Y, Cai W, Liu S, Hu M, Liao S, Huang X, Zhang B, Wang Y, Lu Z (2019) Cerebral small vessel disease: neuroimaging markers and clinical implication. J Neurol 266:2347–2362. https://doi.org/10.1007/s00415-018-9077-3CrossRefPubMed

29.

Mestre H, Kostrikov S, Mehta RI, Nedergaard M (2017) Perivascular spaces, glymphatic dysfunction, and small vessel disease. Clin Sci (Lond) 131:2257–2274. https://doi.org/10.1042/cs20160381CrossRefPubMed

30.

Zeng Q, Li K, Luo X, Wang S, Xu X, Jiaerken Y, Liu X, Hong L, Hong H, Li Z, Fu Y, Zhang T, Chen Y, Liu Z, Huang P, Zhang M (2022) The association of enlarged perivascular space with microglia-related inflammation and Alzheimer’s pathology in cognitively normal elderly. Neurobiol Dis 170:105755. https://doi.org/10.1016/j.nbd.2022.105755CrossRefPubMed

31.

Perosa V, Oltmer J, Munting LP, Freeze WM, Auger CA, Scherlek AA, van der Kouwe AJ, Iglesias JE, Atzeni A, Bacskai BJ, Viswanathan A, Frosch MP, Greenberg SM, van Veluw SJ (2022) Perivascular space dilation is associated with vascular amyloid-β accumulation in the overlying cortex. Acta Neuropathol 143:331–348. https://doi.org/10.1007/s00401-021-02393-1CrossRefPubMed

32.

Liu H, Yang S, He W, Liu X, Sun S, Wang S, Wang Y, Zhou X, Tang T, Xia J, Liu Y, Huang Q (2021) Associations among diffusion tensor image along the perivascular space (DTI-ALPS), enlarged perivascular space (ePVS), and cognitive functions in asymptomatic patients with carotid plaque. Front Neurol 12:789918. https://doi.org/10.3389/fneur.2021.789918CrossRefPubMed

33.

Doubal FN, MacLullich AM, Ferguson KJ, Dennis MS, Wardlaw JM (2010) Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease. Stroke 41:450–454. https://doi.org/10.1161/strokeaha.109.564914CrossRefPubMed

34.

Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol 149:351–356. https://doi.org/10.2214/ajr.149.2.351CrossRefPubMed

35.

Si X, Guo T, Wang Z, Fang Y, Gu L, Cao L, Yang W, Gao T, Song Z, Tian J, Yin X, Guan X, Zhou C, Wu J, Bai X, Liu X, Zhao G, Zhang M, Pu J, Zhang B (2022) Neuroimaging evidence of glymphatic system dysfunction in possible REM sleep behavior disorder and Parkinson’s disease. NPJ Parkinsons Dis 8:54. https://doi.org/10.1038/s41531-022-00316-9CrossRefPubMedPubMedCentral

36.

Andica C, Kamagata K, Hatano T, Saito Y, Ogaki K, Hattori N, Aoki S (2020) MR biomarkers of degenerative brain disorders derived from diffusion imaging. J Magn Reson Imaging 52:1620–1636. https://doi.org/10.1002/jmri.27019CrossRefPubMed

37.

Chandra A, Dervenoulas G, Politis M (2019) Magnetic resonance imaging in Alzheimer’s disease and mild cognitive impairment. J Neurol 266:1293–1302. https://doi.org/10.1007/s00415-018-9016-3CrossRefPubMed

38.

Liheng M, Guofan X, Balzano RF, Yuying L, Weifeng H, Ning Y, Yayun J, Mouyuan L, Guglielmi G (2021) The value of DTI: achieving high diagnostic performance for brain metastasis. Radiol Med 126:291–298. https://doi.org/10.1007/s11547-020-01243-6CrossRefPubMed

39.

Taoka T, Naganawa S (2020) Glymphatic imaging using MRI. J Magn Reson Imaging 51:11–24. https://doi.org/10.1002/jmri.26892CrossRefPubMed

40.

Ma X, Li S, Li C, Wang R, Chen M, Chen H, Su W (2021) Diffusion tensor imaging along the perivascular space index in different stages of Parkinson’s disease. Front Aging Neurosci 13:773951. https://doi.org/10.3389/fnagi.2021.773951CrossRefPubMedPubMedCentral

41.

Chen HL, Chen PC, Lu CH, Tsai NW, Yu CC, Chou KH, Lai YR, Taoka T, Lin WC (2021) Associations among cognitive functions, plasma DNA, and diffusion tensor image along the perivascular space (DTI-ALPS) in patients with Parkinson’s disease. Oxid Med Cell Longev 2021:4034509. https://doi.org/10.1155/2021/4034509CrossRefPubMedPubMedCentral

42.

Shen T, Yue Y, Ba F, He T, Tang X, Hu X, Pu J, Huang C, Lv W, Zhang B, Lai HY (2022) Diffusion along perivascular spaces as marker for impairment of glymphatic system in Parkinson’s disease. NPJ Parkinsons Dis 8:174. https://doi.org/10.1038/s41531-022-00437-1CrossRefPubMedPubMedCentral

43.

Qin Y, He R, Chen J, Zhou X, Zhou X, Liu Z, Xu Q, Guo JF, Yan XX, Jiang N, Liao W, Taoka T, Wang D, Tang B (2023) Neuroimaging uncovers distinct relationships of glymphatic dysfunction and motor symptoms in Parkinson’s disease. J Neurol. https://doi.org/10.1007/s00415-023-11594-5CrossRefPubMedPubMedCentral

44.

Da Mesquita S, Herz J, Wall M, Dykstra T, de Lima KA, Norris GT, Dabhi N, Kennedy T, Baker W, Kipnis J (2021) Aging-associated deficit in CCR7 is linked to worsened glymphatic function, cognition, neuroinflammation, and β-amyloid pathology. Sci Adv 7:21. https://doi.org/10.1126/sciadv.abe4601CrossRef

45.

McKnight CD, Trujillo P, Lopez AM, Petersen K, Considine C, Lin YC, Yan Y, Kang H, Donahue MJ, Claassen DO (2021) Diffusion along perivascular spaces reveals evidence supportive of glymphatic function impairment in Parkinson disease. Parkinsonism Relat Disord 89:98–104. https://doi.org/10.1016/j.parkreldis.2021.06.004CrossRefPubMedPubMedCentral

46.

Kim J, Lee DA, Lee HJ, Park BS, Ko J, Park SH, Lee YJ, Kim IH, Park JH, Park KM (2022) Glymphatic system dysfunction in patients with cluster headache. Brain Behav 12:e2631. https://doi.org/10.1002/brb3.2631CrossRefPubMedPubMedCentral

47.

Lee DA, Park BS, Ko J, Park SH, Park JH, Kim IH, Lee YJ, Park KM (2022) Glymphatic system function in patients with newly diagnosed focal epilepsy. Brain Behav 12:e2504. https://doi.org/10.1002/brb3.2504CrossRefPubMedPubMedCentral

48.

Verghese JP, Terry A, de Natale ER, Politis M (2022) Research evidence of the role of the glymphatic system and its potential pharmacological modulation in neurodegenerative diseases. J Clin Med 11:6964. https://doi.org/10.3390/jcm11236964CrossRefPubMedPubMedCentral

49.

Fang Y, Gu LY, Tian J, Dai SB, Chen Y, Zheng R, Si XL, Jin CY, Song Z, Yan YP, Yin XZ, Pu JL, Zhang BR (2020) MRI-visible perivascular spaces are associated with cerebrospinal fluid biomarkers in Parkinson’s disease. Aging (Albany NY) 12:25805–25818. https://doi.org/10.18632/aging.104200CrossRefPubMed

50.

Sibilia F, Sheikh-Bahaei N, Mack WJ, Choupan J (2023) Perivascular spaces in Alzheimer’s disease are associated with inflammatory, stress-related, and hypertension biomarkers. bioRxiv. https://doi.org/10.1101/2023.06.02.543504CrossRefPubMedPubMedCentral

51.

Bae JH, Kim JM, Park KY, Han SH (2021) Association between arterial stiffness and the presence of cerebral small vessel disease markers. Brain Behav 11:e01935. https://doi.org/10.1002/brb3.1935CrossRefPubMed

52.

Mestre H, Tithof J, Du T, Song W, Peng W, Sweeney AM, Olveda G, Thomas JH, Nedergaard M, Kelley DH (2018) Flow of cerebrospinal fluid is driven by arterial pulsations and is reduced in hypertension. Nat Commun 9:4878. https://doi.org/10.1038/s41467-018-07318-3CrossRefPubMedPubMedCentral

53.

Brown R, Benveniste H, Black SE, Charpak S, Dichgans M, Joutel A, Nedergaard M, Smith KJ, Zlokovic BV, Wardlaw JM (2018) Understanding the role of the perivascular space in cerebral small vessel disease. Cardiovasc Res 114:1462–1473. https://doi.org/10.1093/cvr/cvy113CrossRefPubMedPubMedCentral

54.

Shulyatnikova T, Hayden MR (2023) Why are perivascular spaces important? Medicina (Kaunas) 59:917. https://doi.org/10.3390/medicina59050917CrossRefPubMed

55.

Donahue EK, Murdos A, Jakowec MW, Sheikh-Bahaei N, Toga AW, Petzinger GM, Sepehrband F (2021) Global and regional changes in perivascular space in idiopathic and familial Parkinson’s disease. Mov Disord 36:1126–1136. https://doi.org/10.1002/mds.28473CrossRefPubMedPubMedCentral

56.

Vilor-Tejedor N, Ciampa I, Operto G, Falcón C, Suárez-Calvet M, Crous-Bou M, Shekari M, Arenaza-Urquijo EM, Milà-Alomà M, Grau-Rivera O, Minguillon C, Kollmorgen G, Zetterberg H, Blennow K, Guigo R, Molinuevo JL, Gispert JD (2021) Perivascular spaces are associated with tau pathophysiology and synaptic dysfunction in early Alzheimer’s continuum. Alzheimers Res Ther 13:135. https://doi.org/10.1186/s13195-021-00878-5CrossRefPubMedPubMedCentral

57.

Ma X, Li S, Li C, Wang R, Chen M, Chen H, Su W (2021) Total cerebral small vessel score association with Hoehn and Yahr stage in Parkinson’s disease. Front Aging Neurosci 13:682776. https://doi.org/10.3389/fnagi.2021.682776CrossRefPubMedPubMedCentral

58.

Dubost F, Yilmaz P, Adams H, Bortsova G, Ikram MA, Niessen W, Vernooij M, de Bruijne M (2019) Enlarged perivascular spaces in brain MRI: automated quantification in four regions. Neuroimage 185:534–544. https://doi.org/10.1016/j.neuroimage.2018.10.026CrossRefPubMed

59.

Li Y, Zhu Z, Chen J, Zhang M, Yang Y, Huang P (2020) Dilated perivascular space in the midbrain may reflect dopamine neuronal degeneration in Parkinson’s disease. Front Aging Neurosci 12:161. https://doi.org/10.3389/fnagi.2020.00161CrossRefPubMedPubMedCentral

60.

Gu L, Dai S, Guo T, Si X, Lv D, Wang Z, Lu J, Fang Y, Guan X, Zhou C, Wu H, Xu X, Yan Y, Song Z, Zhang MM, Zhang B, Pu J (2023) Noninvasive neuroimaging provides evidence for deterioration of the glymphatic system in Parkinson’s disease relative to essential tremor. Parkinsonism Relat Disord 107:105254. https://doi.org/10.1016/j.parkreldis.2022.105254CrossRefPubMed

61.

Zhang X, Ding L, Yang L, Qin W, Yuan J, Li S, Hu W (2016) Brain atrophy correlates with severe enlarged perivascular spaces in basal ganglia among lacunar stroke patients. PLoS ONE 11:e0149593. https://doi.org/10.1371/journal.pone.0149593CrossRefPubMedPubMedCentral

62.

Shams S, Martola J, Charidimou A, Larvie M, Granberg T, Shams M, Kristoffersen-Wiberg M, Wahlund LO (2017) Topography and determinants of magnetic resonance imaging (MRI)-visible perivascular spaces in a large memory clinic cohort. J Am Heart Assoc. https://doi.org/10.1161/jaha.117.006279CrossRefPubMedPubMedCentral

63.

Lara FR, Scruton AL, Pinheiro A, Demissie S, Parva P, Charidimou A, Francis M, Himali JJ, DeCarli C, Beiser A, Seshadri S, Romero JR (2022) Aging, prevalence and risk factors of MRI-visible enlarged perivascular spaces. Aging (Albany NY) 14:6844–6858. https://doi.org/10.18632/aging.204181CrossRefPubMed

64.

Sim JE, Park MS, Shin HY, Jang HS, Won HH, Seo SW, Seo WK, Kim BJ, Kim GM (2020) Correlation between hippocampal enlarged perivascular spaces and cognition in non-dementic elderly population. Front Neurol 11:542511. https://doi.org/10.3389/fneur.2020.542511CrossRefPubMedPubMedCentral

65.

Du H, Chen C, Ye C, Lin F, Wei J, Xia P, Chen R, Wu S, Yuan Q, Chen H, Xiao Y, Liu N (2020) Association between steno-occlusive middle cerebral artery and basal ganglia perivascular spaces. Front Neurol 11:293. https://doi.org/10.3389/fneur.2020.00293CrossRefPubMedPubMedCentral

66.

Wang ML, Yu MM, Wei XE, Li WB, Li YH (2021) Association of enlarged perivascular spaces with Aβ and tau deposition in cognitively normal older population. Neurobiol Aging 100:32–38. https://doi.org/10.1016/j.neurobiolaging.2020.12.014CrossRefPubMed

67.

Francis F, Ballerini L, Wardlaw JM (2019) Perivascular spaces and their associations with risk factors, clinical disorders and neuroimaging features: a systematic review and meta-analysis. Int J Stroke 14:359–371. https://doi.org/10.1177/1747493019830321CrossRefPubMed

68.

Hablitz LM, Nedergaard M (2021) The glymphatic system: a novel component of fundamental neurobiology. J Neurosci 41:7698–7711. https://doi.org/10.1523/jneurosci.0619-21.2021CrossRefPubMedPubMedCentral

69.

Bae YJ, Kim JM, Choi BS, Choi JH, Ryoo N, Song YS, Cho SJ, Kim JH (2023) Glymphatic function assessment in Parkinson’s disease using diffusion tensor image analysis along the perivascular space. Parkinsonism Relat Disord 114:105767. https://doi.org/10.1016/j.parkreldis.2023.105767CrossRefPubMed

70.

Ruan X, Huang X, Li Y, Li E, Li M, Wei X (2022) Diffusion tensor imaging analysis along the perivascular space index in primary Parkinson’s disease patients with and without freezing of gait. Neuroscience 506:51–57. https://doi.org/10.1016/j.neuroscience.2022.10.013CrossRefPubMed

71.

Lee DA, Lee HJ, Park KM (2022) Glymphatic dysfunction in isolated REM sleep behavior disorder. Acta Neurol Scand 145:464–470. https://doi.org/10.1111/ane.13573CrossRefPubMed

72.

Bae YJ, Kim JM, Choi BS, Ryoo N, Song YS, Nam Y, Yoon IY, Cho SJ, Kim JH (2023) Altered brain glymphatic flow at diffusion-tensor MRI in rapid eye movement sleep behavior disorder. Radiology 307:e221848. https://doi.org/10.1148/radiol.221848CrossRefPubMed

Title: Correlation of glymphatic system abnormalities with Parkinson’s disease progression: a clinical study based on non-invasive fMRI
Authors: Jing-Cai Meng
Ming-Qiang Shen
Yan-Li Lu
Hong-Xuan Feng
Xin-Yi Chen
Da-Qiang Xu
Guan-Hui Wu
Qing-Zhang Cheng
Lin-Hui Wang
Qian Gui
Publication date: 27-09-2023
Publisher: Springer Berlin Heidelberg
Keyword: Parkinson's Disease
Published in: Journal of Neurology / Issue 1/2024
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-023-12004-6

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Correlation of glymphatic system abnormalities with Parkinson’s disease progression: a clinical study based on non-invasive fMRI

Abstract

Background

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

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