Aqueductal CSF stroke volume is associated with the burden of perivascular space enlargement in chronic adult hydrocephalus.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
05 06 2024
05 06 2024
Historique:
received:
14
09
2023
accepted:
03
06
2024
medline:
6
6
2024
pubmed:
6
6
2024
entrez:
5
6
2024
Statut:
epublish
Résumé
The inflow of CSF into perivascular spaces (PVS) in the brain is crucial for clearing waste molecules. Inefficiency in PVS flow leads to neurodegeneration. Failure of PVS flushing is associated with CSF flow impairment in the intracranial hydrodynamic condition of CSF hypo-pulsatility. However, enlarged PVS (ePVS), a finding indicative of PVS flow dysfunction, is also present in patients with derangement of CSF dynamics characterized by CSF hyper-pulsatility, which increases CSF flow. Intriguingly, two opposite intracranial hydrodynamic conditions would lead to the same result of impairing the PVS flushing. To investigate this issue, we assessed the subsistence of a dysfunctional interplay between CSF and PVS flows and, if the case, the mechanisms preventing a hyper-pulsatile brain from providing an effective PVS flushing. We analyzed the association between phase contrast MRI aqueductal CSF stroke volume (aqSV), a proxy of CSF pulsatility, and the burden of ePVS in chronic adult hydrocephalus, a disease involving a broad spectrum of intracranial hydrodynamics disturbances. In the 147 (85 males, 62 females) patients, the age at diagnosis ranged between 28 and 88 years (median 73 years). Ninety-seven patients had tri-ventriculomegaly and 50 tetra-ventriculomegaly. According to the extent of ePVS, 113 patients had a high ePVS burden, while 34 had a low ePVS burden. aqSV, which ranged between 0 and 562 μL (median 86 μL), was increased with respect to healthy subjects. Patients presenting with less ePVS burden had higher aqSV (p < 0.002, corrected for the multiple comparisons) than those with higher ePVS burden. The present study confirmed the association between CSF dynamics and PVS flow disturbances and demonstrated this association in intracranial hyper-pulsatility. Further studies should investigate the association between PVS flow failure and CSF hypo- and hyper-pulsatility as responsible/co-responsible for glymphatic failure in other neurodegenerative diseases, particularly in diseases in which CSF disturbances can be corrected, as in chronic adult hydrocephalus.
Identifiants
pubmed: 38839864
doi: 10.1038/s41598-024-63926-8
pii: 10.1038/s41598-024-63926-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
12966Informations de copyright
© 2024. The Author(s).
Références
Iliff, J. J. et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci. Transl. Med. 4, 147ra111 (2012).
doi: 10.1126/scitranslmed.3003748
pubmed: 22896675
pmcid: 3551275
Weller, R. O. et al. Cerebral amyloid angiopathy: Amyloid beta accumulates in putative interstitial fluid drainage pathways in Alzheimer’s disease. Am. J. Pathol. 153, 725–733 (1998).
doi: 10.1016/S0002-9440(10)65616-7
pubmed: 9736023
pmcid: 1853019
Iliff, J. J. et al. Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J. Neurosci. 34, 16180–16193 (2014).
doi: 10.1523/JNEUROSCI.3020-14.2014
pubmed: 25471560
pmcid: 4252540
Causemann, M., Vinje, V. & Rognes, M. E. Human intracranial pulsatility during the cardiac cycle: A computational modelling framework. Fluids Barriers CNS 19, 84 (2022).
doi: 10.1186/s12987-022-00376-2
pubmed: 36320038
pmcid: 9623946
Mestre, H. et al. Flow of cerebrospinal fluid is driven by arterial pulsations and is reduced in hypertension. Nat. Commun. 9, 4878 (2018).
doi: 10.1038/s41467-018-07318-3
pubmed: 30451853
pmcid: 6242982
Gallina, P. et al. The “glymphatic–lymphatic system pathology” and a new categorization of neurodegenerative disorders. Front. Neurosci. 15, 669681 (2021).
doi: 10.3389/fnins.2021.669681
pubmed: 34093117
pmcid: 8172792
Gallina, P., Lolli, F., Cianti, D., Perri, F. & Porfirio, B. Failure of the glymphatic system by increases of jugular resistance as possible link between asthma and dementia. Brain Commun. https://doi.org/10.1093/braincomms/fcae039 (2024).
doi: 10.1093/braincomms/fcae039
pubmed: 38410621
pmcid: 10896477
Blair, G. W. Jr. et al. Intracranial hemodynamic relationships in patients with cerebral small vessel disease. Neurology 94, e2258–e2269 (2020).
doi: 10.1212/WNL.0000000000009483
pubmed: 32366534
pmcid: 7357294
Yamada, S. et al. Current and emerging MR imaging techniques for the diagnosis and management of CSF flow disorders: A review of phase-contrast and time–spatial labeling inversion pulse. AJNR Am. J. Neuroradiol. 36, 623–630 (2015).
doi: 10.3174/ajnr.A4030
pubmed: 25012672
pmcid: 7964307
Blitz, A. M. et al. Does phase-contrast imaging through the cerebral aqueduct predict the outcome of lumbar CSF drainage or shunt surgery in patients with suspected adult hydrocephalus?. AJNR Am. J. Neuroradiol. 39, 2224–2230 (2018).
doi: 10.3174/ajnr.A5857
pubmed: 30467214
pmcid: 7655420
Wardlaw, J. M. et al. Perivascular spaces in the brain: Anatomy, physiology and pathology. Nat. Rev. Neurol. 16, 137–153 (2020).
doi: 10.1038/s41582-020-0312-z
pubmed: 32094487
Bradley, W. G. Jr. et al. Normal-pressure hydrocephalus: Evaluation with cerebrospinal fluid flow measurements at MR imaging. Radiology 198, 523–529 (1996).
doi: 10.1148/radiology.198.2.8596861
pubmed: 8596861
Scollato, A. et al. Changes in aqueductal CSF stroke volume and progression of symptoms in patients with unshunted idiopathic normal pressure hydrocephalus. AJNR Am. J. Neuroradiol. 29, 192–197 (2008).
doi: 10.3174/ajnr.A0785
pubmed: 17925364
pmcid: 8119077
Scollato, A. et al. Changes in aqueductal CSF stroke volume in shunted patients with idiopathic normal-pressure hydrocephalus. AJNR Am. J. Neuroradiol. 30, 1580–1586 (2009).
doi: 10.3174/ajnr.A1616
pubmed: 19461060
pmcid: 7051622
Scollato, A. et al. Aqueductal CSF stroke volume measurements may drive management of shunted idiopathic normal pressure hydrocephalus patients. Sci. Rep. 11, 7095 (2021).
doi: 10.1038/s41598-021-86350-8
pubmed: 33782441
pmcid: 8007697
Greitz, D. Cerebrospinal fluid circulation and associated intracranial dynamics: A radiologic investigation using MR imaging and radionuclide cisternography. Acta Radiol. Suppl. 386, 1–23 (1993).
pubmed: 8517189
Naidich, T. P., Altman, N. R. & Gonzalez-Arias, S. M. Phase contrast cine magnetic resonance imaging: Normal cerebrospinal fluid oscillation and applications to hydrocephalus. Neurosurg. Clin. N. Am. 4, 677–705 (1993).
doi: 10.1016/S1042-3680(18)30559-X
pubmed: 8241790
Williams, M. A. et al. The clinical spectrum of hydrocephalus in adults: Report of the first 517 patients of the Adult Hydrocephalus Clinical Research Network registry. Neurosurgery 132, 1773–1784 (2019).
doi: 10.3171/2019.2.JNS183538
Adams, R. D., Fisher, C. M., Hakim, S., Ojemann, R. & Sweet, W. H. Symptomatic occult hydrocephalus with ”normal” cerebrospinal-fluid pressure A treatable syndrome. N. Engl. J. Med. 273, 117–126 (1965).
doi: 10.1056/NEJM196507152730301
pubmed: 14303656
Erten-Lyons, D. et al. Neuropathologic basis of age-associated brain atrophy. JAMA Neurol. 70, 616–622 (2013).
doi: 10.1001/jamaneurol.2013.1957
pubmed: 23552688
pmcid: 3898525
Bateman, G. A., Levi, C. & Schofield, P. W. The pathophysiology of the aqueduct stroke volume in normal pressure hydrocephalus: Can comorbidity with other forms of dementia be excluded?. Neuroradiology 47, 741–748 (2005).
doi: 10.1007/s00234-005-1418-0
pubmed: 16021440
Wagshul, M. E. et al. Amplitude and phase of cerebrospinal fluid pulsations: Experimental studies and review of the literature. J. Neurosurg. 104, 810–819 (2006).
doi: 10.3171/jns.2006.104.5.810
pubmed: 16703889
Stoquart-ElSankari, S. et al. Aging effects on cerebral blood and cerebrospinal fluid flow. J. Cereb. Blood Flow Metab. 27, 1563–1572 (2007).
doi: 10.1038/sj.jcbfm.9600462
pubmed: 17311079
Shanks, J. et al. Aqueductal CSF stroke volume is increased in patients with idiopathic normal pressure hydrocephalus and decreases after shunt surgery. AJNR Am. J. Neuroradiol. 40, 453–459 (2019).
pubmed: 30792248
pmcid: 7028668
Bergsneider, M., Miller, C., Vespa, P. M. & Hu, X. Surgical management of adult hydrocephalus. Neurosurgery 62(Suppl 2), 643–659 (2008).
pubmed: 18596440
Bradley, W. G. Jr., Kortman, K. E. & Burgoyne, B. Flowing cerebrospinal fluid in normal pressure hydrocephalic states: Appearance on MR images. Radiology 159, 611–616 (1986).
doi: 10.1148/radiology.159.3.3704142
pubmed: 3704142
Wu, Y. T. et al. The changing prevalence and incidence of dementia over time—Current evidence. Nat. Rev. Neurol. 13, 327–339 (2017).
doi: 10.1038/nrneurol.2017.63
pubmed: 28497805
Run, L. et al. Characterizing cerebrospinal fluid mobility using heavily T2-weighted 3D fast spin echo (FSE) imaging with improved multi-directional diffusion-sensitized driven-equilibrium (iMDDSDE) preparation. J. Cereb. Blood Flow Metab. 44, 105–117 (2024).
doi: 10.1177/0271678X231194863
Schwartz, D. L. et al. Autoidentification of perivascular spaces in white matter using clinical field strength T1 and FLAIR MR imaging. Neuroimage 202, 116126 (2019).
doi: 10.1016/j.neuroimage.2019.116126
pubmed: 31461676
Ringstad, G., Vatnehol, S. A. S. & Eide, P. K. Glymphatic MRI in idiopathic normal pressure hydrocephalus. Brain 140, 2691–2705 (2017).
doi: 10.1093/brain/awx191
pubmed: 28969373
pmcid: 5841149
Gallina, P. et al. Accuracy and safety of 1-day external lumbar drainage of CSF for shunt selection in patients with idiopathic normal pressure hydrocephalus. J. Neurosurg. 1, 1–7 (2018).