Functional analysis of the human perivascular subarachnoid space.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
05 Mar 2024
05 Mar 2024
Historique:
received:
26
04
2023
accepted:
20
02
2024
medline:
6
3
2024
pubmed:
6
3
2024
entrez:
5
3
2024
Statut:
epublish
Résumé
The human subarachnoid space harbors the cerebrospinal fluid, which flows within a landscape of blood vessels and trabeculae. Functional implications of subarachnoid space anatomy remain far less understood. This study of 75 patients utilizes a cerebrospinal fluid tracer (gadobutrol) and consecutive magnetic resonance imaging to investigate features of early (i.e. within 2-3 h after injection) tracer propagation within the subarachnoid space. There is a time-dependent perivascular pattern of enrichment antegrade along the major cerebral artery trunks; the anterior-, middle-, and posterior cerebral arteries. The correlation between time of first enrichment around arteries and early enrichment in nearby cerebral cortex is significant. These observations suggest the existence of a compartmentalized subarachnoid space, where perivascular ensheathment of arteries facilitates antegrade tracer passage towards brain tissue. Periarterial transport is impaired in subjects with reduced intracranial pressure-volume reserve capacity and in idiopathic normal pressure hydrocephalus patients who also show increased perivascular space size.
Identifiants
pubmed: 38443374
doi: 10.1038/s41467-024-46329-1
pii: 10.1038/s41467-024-46329-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2001Informations de copyright
© 2024. The Author(s).
Références
Weller, R. O., Sharp, M. M., Christodoulides, M., Carare, R. O. & Møllgård, K. The meninges as barriers and facilitators for the movement of fluid, cells and pathogens related to the rodent and human CNS. Acta Neuropathol. 135, 363–385 (2018).
doi: 10.1007/s00401-018-1809-z
Louveau, A. et al. Structural and functional features of central nervous system lymphatic vessels. Nature 523, 337–341 (2015).
doi: 10.1038/nature14432
Aspelund, A. et al. A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J. Exp. Med. 212, 991–999 (2015).
doi: 10.1084/jem.20142290
Nauen, D. W. & Troncoso, J. C. Amyloid-beta is present in human lymph nodes and greatly enriched in those of the cervical region. Alzheimer’s Dement.: J. Alzheimer’s Assoc. 18, 205–210 (2022).
doi: 10.1002/alz.12385
Rustenhoven, J. & Kipnis, J. Brain borders at the central stage of neuroimmunology. Nature 612, 417–429 (2022).
doi: 10.1038/s41586-022-05474-7
Mazzitelli, J. A. et al. Cerebrospinal fluid regulates skull bone marrow niches via direct access through dural channels. Nat. Neurosci. 25, 555–560 (2022).
doi: 10.1038/s41593-022-01029-1
Da Mesquita, S. et al. Meningeal lymphatics affect microglia responses and anti-Aβ immunotherapy. Nature 593, 255–260 (2021).
doi: 10.1038/s41586-021-03489-0
Møllgård, K. et al. A mesothelium divides the subarachnoid space into functional compartments. Science 379, 84–88 (2023).
doi: 10.1126/science.adc8810
Lu, S., Brusic, A. & Gaillard, F. Arachnoid Membranes: Crawling Back into Radiologic Consciousness. Ajnr. Am. J. Neuroradiol. 43, 167–175 (2022).
doi: 10.3174/ajnr.A7309
Rasmussen, M. K., Mestre, H. & Nedergaard, M. Fluid transport in the brain. Physiol. Rev. 102, 1025–1151 (2022).
doi: 10.1152/physrev.00031.2020
Ringstad, G. et al. Brain-wide glymphatic enhancement and clearance in humans assessed with MRI. JCI insight 3, 1–16 (2018).
doi: 10.1172/jci.insight.121537
Eide, P. K. et al. Intrathecal Contrast-Enhanced Magnetic Resonance Imaging of Cerebrospinal Fluid Dynamics and Glymphatic Enhancement in Idiopathic Normal Pressure Hydrocephalus. Front. Neurol. 13, 857328 (2022).
doi: 10.3389/fneur.2022.857328
Ringstad, G. & Eide, P. K. Cerebrospinal fluid tracer efflux to parasagittal dura in humans. Nat. Commun. 11, 354 (2020).
doi: 10.1038/s41467-019-14195-x
Iliff, J. J. et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci. Transl. Med. 4, 147ra111 (2012).
doi: 10.1126/scitranslmed.3003748
Evensen, K. B. & Eide, P. K. Measuring intracranial pressure by invasive, less invasive or non-invasive means: limitations and avenues for improvement. Fluids barriers CNS 17, 1–33 (2020).
doi: 10.1186/s12987-020-00195-3
Eide, P. K. The correlation between pulsatile intracranial pressure and indices of intracranial pressure-volume reserve capacity: results from ventricular infusion testing. J. Neurosurg. 125, 1493–1503 (2016).
doi: 10.3171/2015.11.JNS151529
Eide, P. K. & Sorteberg, W. Diagnostic intracranial pressure monitoring and surgical management in idiopathic normal pressure hydrocephalus: a 6-year review of 214 patients. Neurosurgery 66, 80–91 (2010).
doi: 10.1227/01.NEU.0000363408.69856.B8
Adeeb, N. et al. The intracranial arachnoid mater: a comprehensive review of its history, anatomy, imaging, and pathology. Childs Nerv. Syst. 29, 17–33 (2013).
doi: 10.1007/s00381-012-1910-x
Yasargil, M. G., Kasdaglis, K., Jain, K. K. & Weber, H. P. Anatomical observations of the subarachnoid cisterns of the brain during surgery. J. Neurosurg. 44, 298–302 (1976).
doi: 10.3171/jns.1976.44.3.0298
Rhoton, A. L. Jr. The posterior fossa cisterns. Neurosurgery 47, S287–S297 (2000).
doi: 10.1097/00006123-200009001-00029
Key, A., Retzius, G. Studien in der Anatomie des Nervensystems und des Bindegewebes (Samson and Wallin, Stockholm, 1875).
Liliequist, B. The anatomy of the subarachnoid cisterns. Acta Radio. 46, 61–71 (1956).
doi: 10.3109/00016925609170813
Froelich, S. C., Abdel Aziz, K. M., Cohen, P. D., van Loveren, H. R. & Keller, J. T. Microsurgical and endoscopic anatomy of Liliequist’s membrane: a complex and variable structure of the basal cisterns. Neurosurgery 63, ONS1–ONS8 (2008). discussion ONS8-9.
Alcolado, R., Weller, R. O., Parrish, E. P. & Garrod, D. The cranial arachnoid and pia mater in man: anatomical and ultrastructural observations. Neuropathol. Appl. Neurobiol. 14, 1–17 (1988).
doi: 10.1111/j.1365-2990.1988.tb00862.x
Zhang, E. T., Inman, C. B. & Weller, R. O. Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J. Anat. 170, 111–123 (1990).
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
Abbott, N. J., Pizzo, M. E., Preston, J. E., Janigro, D. & Thorne, R. G. The role of brain barriers in fluid movement in the CNS: is there a ‘glymphatic’ system? Acta Neuropathol. 135, 387–407 (2018).
doi: 10.1007/s00401-018-1812-4
Edeklev, C. S. et al. Intrathecal Use of Gadobutrol for Glymphatic MR Imaging: Prospective Safety Study of 100 Patients. Ajnr. Am. J. Neuroradiol. 40, 1257–1264 (2019).
doi: 10.3174/ajnr.A6136
Iliff, J. J. et al. Cerebral arterial pulsation drives paravascular CSF-interstitial fluid exchange in the murine brain. J. Neurosci. 33, 18190–18199 (2013).
doi: 10.1523/JNEUROSCI.1592-13.2013
Lohela, T. J., Lilius, T. O. & Nedergaard, M. The glymphatic system: implications for drugs for central nervous system diseases. Nat. Rev. Drug Discov. 21, 763–779 (2022).
doi: 10.1038/s41573-022-00500-9
Suzuki, H. et al. Aging-associated inflammation and fibrosis in arachnoid membrane. BMC Neurol. 21, 169 (2021).
doi: 10.1186/s12883-021-02202-y
Plog, B. A. et al. Biomarkers of traumatic injury are transported from brain to blood via the glymphatic system. J. Neurosci. 35, 518–526 (2015).
doi: 10.1523/JNEUROSCI.3742-14.2015
Kress, B. T. et al. Impairment of paravascular clearance pathways in the aging brain. Ann. Neurol. 76, 845–861 (2014).
doi: 10.1002/ana.24271
Eide, P. K. et al. Pressure-derived versus pressure wave amplitude-derived indices of cerebrovascular pressure reactivity in relation to early clinical state and 12-month outcome following aneurysmal subarachnoid hemorrhage. J. Neurosurg. 116, 961–971 (2012).
doi: 10.3171/2012.1.JNS111313
Evensen, K. B. & Eide, P. K. Mechanisms behind altered pulsatile intracranial pressure in idiopathic normal pressure hydrocephalus: role of vascular pulsatility and systemic hemodynamic variables. Acta Neurochir. (Wien.) 162, 1803–1813 (2020).
doi: 10.1007/s00701-020-04423-5
Mutsaers, S. E., Pixley, F. J., Prêle, C. M. & Hoyne, G. F. Mesothelial cells regulate immune responses in health and disease: role for immunotherapy in malignant mesothelioma. Curr. Opin. Immunol. 64, 88–109 (2020).
doi: 10.1016/j.coi.2020.04.005
Jiménez-Altayó, F. et al. Arachnoid membrane as a source of sphingosine-1-phosphate that regulates mouse middle cerebral artery tone. J. Cereb. Blood Flow. Metab. 42, 162–174 (2022).
doi: 10.1177/0271678X211033362
Segonne, F. et al. A hybrid approach to the skull stripping problem in MRI. Neuroimage 22, 1060–1075 (2004).
doi: 10.1016/j.neuroimage.2004.03.032
Fischl, B. et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355 (2002).
doi: 10.1016/S0896-6273(02)00569-X
Fischl, B. et al. Sequence-independent segmentation of magnetic resonance images. Neuroimage 23, S69–S84 (2004).
doi: 10.1016/j.neuroimage.2004.07.016