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Cited by 293Cerebrospinal fluid and hydrocephalusCerebral Venous Sinus ThrombosisNeurosurgical Procedures and Complications

Cerebrospinal fluid tracer efflux to parasagittal dura in humans

Open access
Ringstad, Geir, Eide, Per Kristian·2020·Nature Communications
DOI 10.1038/s41467-019-14195-xPMC PMC6969040
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Abstract

The mechanisms behind molecular transport from cerebrospinal fluid to dural lymphatic vessels remain unknown. This study utilized magnetic resonance imaging along with cerebrospinal fluid tracer to visualize clearance pathways to human dural lymphatics in vivo. In 18 subjects with suspicion of various types of cerebrospinal fluid disorders, 3D T2-Fluid Attenuated Inversion Recovery, T1-black-blood, and T1 gradient echo acquisitions were obtained prior to intrathecal administration of the contrast agent gadobutrol (0.5 ml, 1 mmol/ml), serving as a cerebrospinal fluid tracer. Propagation of tracer was followed with T1 sequences at 3, 6, 24 and 48 h after the injection. The tracer escaped from cerebrospinal fluid into parasagittal dura along the superior sagittal sinus at areas nearby entry of cortical cerebral veins. The findings demonstrate that trans-arachnoid molecular passage does occur and suggest that parasagittal dura may serve as a bridging link between human brain and dural lymphatic vessels.

AI snapshot

Written from the paper’s full text.

TL;DR

In 18 patients with suspected cerebrospinal fluid (CSF) disorders, intrathecal gadobutrol tracer was followed by MRI for up to 48 h and escaped from CSF into parasagittal dura along the superior sagittal sinus. The findings suggest parasagittal dura may bridge molecular exchange between brain/CSF and dural lymphatic vessels in humans.

Key findings

  • Parasagittal dura was identified in 18/18 patients; after intrathecal gadobutrol, normalized T1-BB signal increased in parasagittal dura at 6, 24, and 48 h, peaking at 24 h (mean percentage change from pre: 156 ± 148 at 6 h, 194 ± 188 at 24 h, 98 ± 79 at 48 h; Table 2).
  • At group level, signal change was highly significant in both parasagittal dura and nearby CSF, was largest within CSF, and signal increases in CSF and parasagittal dura were highly associated (R = 0.92, P < 0.001), with strong positive correlation at all time points.
  • Tracer enhancement below skull base outlets was visually detected below the hypoglossal canal in 17/18, the jugular foramen in 17/18, the cribriform plate in 2/18, and the foramen ovale in 0/18.
  • Tubular structures resembling dural lymphatic vessels could not be discriminated from other enhancing parasagittal dura tissue, possibly related to the 1 × 1 × 1 mm MRI voxel resolution.

Methods

  • Prospective observational study of 18 consecutive individuals referred to neurosurgery for various CSF circulation disorders; no randomization or a priori sample size calculation was used. Exclusion criteria included contrast hypersensitivity, severe allergy, renal dysfunction, age <18 or >80 years, and pregnancy/breastfeeding.
  • Scans were obtained on a 3-Tesla MRI with 3D T2-FLAIR, T1-black-blood, and T1-gradient echo acquisitions; T1-weighted scans were repeated at 3, 6, 24, and 48 h after intrathecal injection of 0.5 ml gadobutrol (1 mmol/ml), preceded by iodixanol to confirm needle position.
  • Regions of interest were placed in parasagittal dura and adjacent subarachnoid CSF on T1-black-blood images, normalized against the ocular bulb vitreous body; differences used linear mixed models with random intercept, correlations used Pearson coefficient, and significance was set at 0.05.

Limitations

  • Stated in the paper: MRI resolution was limited to 1 mm voxel size; lack of T1-mapping techniques restricted measures to semi-quantitative tracer enrichment; the ocular bulb reference may be affected by motion artifacts; and the 48-h multi-phase protocol limited the number of scans per patient, making the peak enhancement time a rough estimate.
  • Evident from the text: the cohort was small (18 patients) and clinically heterogeneous, with no healthy controls; the study could not resolve dural lymphatic vessels directly or quantify the relative importance of parasagittal versus basal outflow pathways.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1038/s41467-019-14195-x

Cites

23 of 23 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 26 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    CSF tracer enhanced in macroscopically visible arachnoid granulations bulging into the sagittal sinus in scattered locations.

    “As expected, CSF tracer also enhanced in macroscopically visible arachnoid granulations, bulging into the sagittal sinus in scattered locations”
    Quote in the paperNot a substantial claim
  • Findingown data

    At late scans (24 and 48 h), remnants of tracer in CSF typically accumulated at high cerebral convexities and in regions adjacent to parasagittal dura.

    “At late scans (i.e. 24 and 48 h, respectively), the remnants of tracer in CSF typically accumulated at the high cerebral convexities and in regions adjacent to parasagittal dura”
    Quote in the paperNot a substantial claim
  • Findingown data

    Tracer enrichment in parasagittal dura was highly dependent on presence of tracer in adjacent CSF, shown by strong positive correlation at all time points (3, 6, 24 and 48 h).

    “The tracer enrichment in parasagittal dura was highly dependent on presence of tracer in adjacent CSF, which was shown by their strong positive correlation at all time points (3, 6, 24 and 48 h)”
    Quote in the paperSubstantial claim
  • Findingown data

    Parasagittal dura tissue with defined MRI features was visually identified almost exclusively along the middle to posterior segment of the superior sagittal sinus, corresponding to levels where cortical veins enter the sinus.

    “Tissue within the parasagittal dura having features as specified above (intermediate or high signal at T2-FLAIR (not free CSF) and at T1-BB (not blood)) was visually identified almost exclusively along the middle to posterior segment of the superior sagittal sinus (Fig. 1; Supplementary Movie 2), corresponding well with the levels where cortical veins enter the sinus.”
    Quote in the paperSubstantial claim
  • Findingown data

    The region with tracer enhancement stretches laterally to a larger extent than can be anticipated from previous anatomical descriptions of intradural human arachnoid granulations.

    “The region with tracer enhancement, as presented here, stretches laterally to a larger extent than what can be anticipated from the previous anatomical descriptions of intradural human arachnoid granulations14,15”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [14] Han, H., Tao, W. & Zhang, M. The dural entrance of cerebral bridging veins into the superior sagittal sinus: an anatomical comparison between cadavers and digital subtraction angiography. Neuroradiology 49, 169–175 (2007). source

      Not checked in the free run.

    • cites [15] Fox, R. J., Walji, A. H., Mielke, B., Petruk, K. C. & Aronyk, K. E. Anatomic details of intradural channels in the parasagittal dura: a possible pathway for flow of cerebrospinal fluid. Neurosurgery 39, 84–90 (1996). source

      Not checked in the free run.

  • May combine two claims. 17
  • Classified as probably not a substantial claim. 16
  • The quote only partly states this claim. 1

  • May combine two claims.

    Findingown data

    Parasagittal dura tissue with defined features was depicted in 18/18 study patients and had typical appearance of longitudinally interspersed areas up to several millimeters transversal width.

    “Even though there were some variations with regard to prominence, tissue in parasagittal dura with features as here defined was depicted in 18/18 study patients and had the typical appearance of longitudinally interspersed areas of up to several millimeters’ transversal width”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Signal change peaked at 24 h in both CSF and PSD, and signal increase in these structures was highly associated (R = 0.92, P < 0.001).

    “Also note that signal change peaked at 24 h in both CSF and PSD, and signal increase in these structures was highly associated (R = 0.92, P < 0.001).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    At group level, normalized T1 signal units within parasagittal dura increased significantly, though increase was more pronounced in nearby CSF.

    “At group level, there was a highly significant increase in normalized T1 signal units within the parasagittal dura, though more pronounced in nearby CSF”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    After intrathecal CSF tracer, parasagittal dura enrichment occurred at 6, 24, and 48 h, peaking at 24 h.

    “After intrathecal injection of CSF tracer, we found enrichment of parasagittal dura at 6, 24 and 48 h and with peak at 24 h”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Tracer enhancement on T1-BB below cranial nerve outlets at skull base was detected below hypoglossal canal in 17/18, jugular foramen in 17/18, cribriform plate in 2/18, and foramen ovale in 0/18 individuals.

    “For the visual assessment of tracer enhancement on T1-BB below selected cranial nerve outlets at the skull base, this was detected below the hypoglossal canal in 17/18, the jugular foramen in 17/18, the cribriform plate in 2/18, and the foramen ovale in 0/18 individuals”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    True lymphatic vessels reside within the dura mater.

    “true lymphatic vessels were shown to reside within the dura mater3,4”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [3] Aspelund, A. et al. A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J. Exp. Med. 212, 991–999 (2015). source

      Not checked in the free run.

    • cites [4] Louveau, A. et al. Structural and functional features of central nervous system lymphatic vessels. Nature 523, 337–341 (2015). source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    It seems plausible that molecules within parasagittal dura structures may reach adjacent lymphatic vessels, and perhaps also vice versa.

    “it seems plausible that molecules within parasagittal dura structures may well reach adjacent lymphatic vessels, and perhaps also vice versa”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [3] Aspelund, A. et al. A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J. Exp. Med. 212, 991–999 (2015). source

      Not checked in the free run.

    • cites [4] Louveau, A. et al. Structural and functional features of central nervous system lymphatic vessels. Nature 523, 337–341 (2015). source

      Not checked in the free run.

    • cites [16] Mastorakos, P. & McGavern, D. The anatomy and immunology of vasculature in the central nervous system. Sci. Immunol. 4, eaav0492 (2019). source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationcitation

    Previous findings showing impairment of meningeal lymphatic function slows paravascular influx and efflux may suggest that impaired lymphatic clearance function exerts negative effect directly on accumulation of molecules within CSF, and upstream on molecular exit from brain into CSF.

    “previous findings showing that impairment of meningeal lymphatic function slows paravascular influx of macromolecules into the brain, as well as efflux from the interstitial space5, may suggest that impaired lymphatic clearance function may exert its negative effect directly on the accumulation of molecules within the CSF, and thereby further upstream on molecular exit from brain into CSF”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [5] Da Mesquita, S. et al. Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease. Nature 560, 185–191 (2018). source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Tracer escape occurs to dura outside arachnoid granulations and into the network of intradural channels.

    “which should be highly suggestive for tracer escape to dura outside arachnoid granulations and into the network of intradural channels”
    Quote in the paperSubstantial claim

  • May combine two claims. The quote only partly states this claim.

    Interpretationreasoning

    The current findings compare better with previous anatomical reports of parasagittal dura microstructure than with dural lymphatic vessel or arachnoid granulation MRI appearances.

    “Our findings compare better with previous anatomical reports demonstrating that parasagittal dura along the middle one-third of the superior sagittal sinus harbors a dense carpet of arachnoid granulations medially”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Impairment of meningeal lymphatic pathways slows paravascular efflux of amyloid-β from interstitial brain fluid.

    “impairment of these meningeal lymphatic pathways has been shown to slow paravascular efflux of amyloid-β from interstitial brain fluid”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [5] Da Mesquita, S. et al. Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease. Nature 560, 185–191 (2018). source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductreasoning

    The long duration of molecular clearance from human CSF and high demand on patients/resources associated with multi-phase MR imaging over 48 h limited the number of scans per patient.

    “Moreover, the long duration of molecular clearance from human CSF, and the high demand on patients and resources associated with multi-phase MR imaging over 48 h, has limited the number of scans we were able to perform in single patients through this time span.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductreasoning

    In the lack of T1-mapping techniques with image resolution close to 1 mm, the study could not go beyond semi-quantitative measures of tracer enrichment.

    “In the lack of T1-mapping techniques with image resolution even close to 1 mm, we did not have the opportunity to go beyond semi-quantitative measures of tracer enrichment.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    A recent animal study was unable to reproduce passage of CSF tracer into dural lymphatic vessels.

    “A recent animal study was, however, unable to reproduce passage of CSF tracer into dural lymphatic vessels7”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [7] Ma, Q., Ineichen, B. V., Detmar, M. & Proulx, S. T. Outflow of cerebrospinal fluid is predominantly through lymphatic vessels and is reduced in aged mice. Nat. Commun. 8, 1434 (2017). source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    The human subarachnoid space is continuous with the paravascular compartment of all brain regions.

    “The human subarachnoid space is shown to be continuous with the paravascular compartment of all brain regions1”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [1] Ringstad, G. et al. Brain-wide glymphatic enhancement and clearance in humans assessed with MRI. JCI Insight 3, 121537 (2018). source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    In rats, from total amount of MRI contrast agent injected into cisterna magna, merely 19% enriched brain parenchyma, remainder escaped via other routes.

    “It has, however, been demonstrated in rats that from the total amount of MRI contrast agent injected into the cisterna magna, merely 19% enriched the brain parenchyma, the remainder escaped via other routes22.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [22] Lee, H. et al. Quantitative Gd-DOTA uptake from cerebrospinal fluid into rat brain using 3D VFA-SPGR at 9.4T. Magn. Reson. Med. 79, 1568–1578 (2018). source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Previous observations indicate that the arachnoid constitutes an impermeable barrier layer between CSF and dura mater.

    “previous observations indicating that the arachnoid constitutes an impermeable barrier layer between the CSF and dura mater8,9”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [8] Nabeshima, S., Reese, T. S., Landis, D. M. & Brightman, M. W. Junctions in the meninges and marginal glia. J. Comp. Neurol. 164, 127–169 (1975). source

      Not checked in the free run.

    • cites [9] Coles, J. A., Myburgh, E., Brewer, J. M. & McMenamin, P. G. Where are we? The anatomy of the murine cortical meninges revisited for intravital imaging, immunology, and clearance of waste from the brain. Prog. Neurobiol. 156, 107–148 (2017). source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Previous anatomical reports demonstrate that parasagittal dura along middle one-third of superior sagittal sinus harbors a dense carpet of arachnoid granulations medially, in close association with an extensive network of intradural channels from 0.02 to 2.0 mm in diameter, coursing and coalescing into lateral lacunae from laterally toward the superior sagittal sinus.

    “Our findings compare better with previous anatomical reports demonstrating that parasagittal dura along the middle one-third of the superior sagittal sinus harbors a dense carpet of arachnoid granulations medially, being in close association with an extensive network of intradural channels from 0.02 to 2.0 mm in diameter, coursing and coalescing into lateral lacunae from laterally toward the super”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [13] Mack, J., Squier, W. & Eastman, J. T. Anatomy and development of the meninges: implications for subdural collections and CSF circulation. Pediatr. Radiol. 39, 200–210 (2009). source

      Not checked in the free run.

    • cites [14] Han, H., Tao, W. & Zhang, M. The dural entrance of cerebral bridging veins into the superior sagittal sinus: an anatomical comparison between cadavers and digital subtraction angiography. Neuroradiology 49, 169–175 (2007). source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The in vivo MRI observations show that parasagittal dura does not drain CSF only, but also molecules, with high dependence on their presence in adjacent subarachnoid compartment.

    “The in vivo-based observations from the current MRI study show that parasagittal dura does not drain CSF only, but also molecules, with high level of dependence on their presence in the adjacent subarachnoid compartment.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    An obvious limitation of this study is the MR image resolution of 1 mm voxel size.

    “An obvious limitation of this study is the MR image resolution of 1 mm voxel size.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    The study corroborates findings from animal studies by showing that CSF molecular outflow through skull base foramina occurs also in humans.

    “While our study corroborates findings from animal studies by showing that CSF molecular outflow through skull base foramina occurs also in humans”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    The extent of enhancing tissue within parasagittal dura does not resemble previously reported appearance of true dural lymphatic vessels (tubular-shaped, sub-millimeter, near venous sinus wall) nor classical MRI appearance of arachnoid granulations bulging into venous sinuses.

    “The extent of enhancing tissue within parasagittal dura does not resemble the previously reported appearance of true dural lymphatic vessels, which are tubular-shaped structures of sub-millimeter cross-sectional diameter near the venous sinus wall3,4,11, and also far from the classical MRI appearance of arachnoid granulations bulging into venous sinuses12.”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [3] Aspelund, A. et al. A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J. Exp. Med. 212, 991–999 (2015). source

      Not checked in the free run.

    • cites [4] Louveau, A. et al. Structural and functional features of central nervous system lymphatic vessels. Nature 523, 337–341 (2015). source

      Not checked in the free run.

    • cites [11] Absinta, M. et al. Human and nonhuman primate meninges harbor lymphatic vessels that can be visualized noninvasively by MRI. eLife 6, e29738 (2017). source

      Not checked in the free run.

    • cites [12] Trimble, C. R., Harnsberger, H. R., Castillo, M., Brant-Zawadzki, M. & Osborn, A. G. “Giant” arachnoid granulations just like CSF?: NOT!! AJNR Am. J. Neuroradiol. 31, 1724–1728 (2010). source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    The inability to discriminate tubular structures resembling dural lymphatic vessels may be related to the image resolution of MRI scans being restricted to 1 × 1 × 1 mm voxel size.

    “may be related to the image resolution of our MRI scans being restricted to 1 × 1 × 1 mm voxel size”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductreasoning

    The time point for peak tracer enhancement in human parasagittal dura must be considered a rough estimate.

    “Therefore, the time point for peak tracer enhancement in human parasagittal dura must be considered to represent a rough estimate.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductreasoning

    The ocular bulbs may be affected by some motion artifacts during scans of several minutes, so an extra-cranial device would ideally have been used as reference for normalization.

    “Ideally, we could also have used an extra-cranial device as reference for normalization of signal units, as the ocular bulbs may be affected by some motion artifacts during scans of several minutes.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Gadobutrol is a non-ionic, highly hydrophilic molecule of relatively small size (604 Da), prevented by the intact brain-blood-barrier from leakage into CNS blood vessels when administered intrathecally.

    “Gadobutrol is a non-ionic, highly hydrophilic molecule of relatively small size (604 Da), prevented by the intact brain–blood–barrier from leakage into CNS blood vessels when administered intrathecally10.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [10] Cheng, K. T. Gadobutrol. in Molecular Imaging and Contrast Agent Database (MICAD) (National Center for Biotechnology Information, Bethesda, USA, 2004). https://www.ncbi.nlm.nih.gov/pubmed/20641787.

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The endothelium of intradural channels was proposed to possibly be the final barrier for absorption of CSF to venous blood, but passage of CSF over this cell layer has never since been confirmed in vivo.

    “The endothelium of intradural channels was proposed to possibly be the final barrier for the absorption of CSF to venous blood15, but passage of CSF over this cell layer has never since been confirmed in vivo.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [15] Fox, R. J., Walji, A. H., Mielke, B., Petruk, K. C. & Aronyk, K. E. Anatomic details of intradural channels in the parasagittal dura: a possible pathway for flow of cerebrospinal fluid. Neurosurgery 39, 84–90 (1996). source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Neurotoxic molecules such as amyloid-β and tau are cleared from brain tissue along paravenous pathways (the glymphatic system).

    “It has previously been shown that neurotoxic molecules such as amyloid-β and tau are cleared from brain tissue along paravenous pathways (the glymphatic system)20”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [20] 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). source

      Not checked in the free run.

28 of 28

  • The paper relies on this without support.

    The olfactory system is proportionally much lesser in size in humans than in rodents.

    “The olfactory system is indeed of proportionally much lesser size in humans than in rodents”

  • The paper relies on this without support.

    The observed CSF tracer efflux in patients with suspected CSF disorders reflects normal human CSF clearance physiology.

    “The study included 18 patients who were under clinical work-up for possible CSF disorders of various etiologies”
    “In 18 subjects with suspicion of various types of cerebrospinal fluid disorders”

  • The paper relies on this without support.

    T1 signal change in parasagittal dura reflects gadobutrol tracer concentration or enrichment.

    “The CSF tracer enrichment was measured as change in T1-BB signal units, and was normalized against the reference (i.e. the vitreous body of the ocular bulb) to correct for any baseline shift of image grayscale between time points”
3 of 3

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Gene ontology and KEGG pathway analysis with upregulated genes in the absence of neuronal IL-17a signaling reveals enriched processes involved in GABA-benzodiazepine activity.

    “Gene ontology and KEGG pathway analysis performed with upregulated genes in the absence of neuronal IL-17a signaling revealed several enriched processes involved in γ-aminobutyric acid (GABA)-benzodiazepine activity (Fig. 6f, Extended Data Fig. 6i), the prototypical target system for anxiolytic drugs15.”

    From Meningeal γδ T cells regulate anxiety-like behavior via IL-17a signaling in neurons (2020) · cites this paper as [15]

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. Cheng, K. T. Gadobutrol. in Molecular Imaging and Contrast Agent Database (MICAD) (National Center for Biotechnology Information, Bethesda, USA, 2004). https://www.ncbi.nlm.nih.gov/pubmed/20641787.

Cited by

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Related

Authors
Ringstad, G., & Eide, P. K.
Affiliations
Oslo University Hospital (NO)
Corresponding author
Eide, Per Kristian
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2020-01-17
Volume
11
Issue
1
Pages
354-354
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-019-14195-x
PMC
PMC6969040
OpenAlex
W3000117238
Semantic Scholar
4ebc1d939b7f614713ef61edcc2b62fdfbbad002
Cited by
292
References
23
Citations by year
2026: 42 · 2025: 50 · 2024: 53 · 2023: 54 · 2022: 45 · 2021: 33 · 2020: 15
FWCI
16.85
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • NORA - Norwegian Open Research Archives (submittedVersion, cc-by)
Funders
Universitetet i Oslo
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Cerebrospinal fluid and hydrocephalus
  • Health Sciences › Medicine › Neurology › Cerebral Venous Sinus Thrombosis
  • Health Sciences › Medicine › Neurology › Neurosurgical Procedures and Complications
Keywords
cerebrospinal fluid, superior sagittal sinus, gadobutrol, cerebrospinal fluid clearance, cerebral veins
MeSH terms
Adult, Aged, Arachnoid, Biological Transport, Brain, Cerebrospinal Fluid, Contrast Media, Dura Mater, Humans, Lymphatic System, Magnetic Resonance Imaging, Middle Aged, Organometallic Compounds, Lymphatic Vessels, Young Adult

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