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Three-dimensional T1 mapping demonstrates the transfer of oxygen into cerebrospinal fluid during hyperoxia

Emma BiondettiiD, Davide Di CensoiD, Sara PomanteiD, Stefano T. CensiiD, Ekaterina BliakharskaiaiD, Manuela CarrieroiD, Lucie ChaletiD, Giulia RoccoiD, Guido BuonincontriiD, Francesca GrazianoiD, Alessandra Stella CaporaleiD, Antonio Maria ChiarelliiD, Richard G. WiseiD

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Abstract

Background: This study optimised a non-invasive magnetic resonance imaging technique to investigate the transfer of oxygen into cerebrospinal fluid (CSF) across the whole brain of healthy subjects. Methods: A shortening of the T1 (longitudinal relaxation time) of CSF was induced by 100% hyperoxia and measured using a 3D SPACE sequence at 3T in 29 subjects, thereby demonstrating the diffusion of oxygen from blood to CSF. T1 mapping was performed at high resolution (0.9-mm isotropic, taking approximately 16 minutes) to capture anatomical details of the CSF spaces and was also repeated more rapidly at a lower resolution (3-mm isotropic, taking approximately 3.5 minutes) to capture the temporal dynamics of T1 changes. Results: Significant region-dependent reductions in T1 were observed, indicating increased oxygen concentration in CSF. These occurred most prominently and rapidly in the cortical subarachnoid space and basilar cisterns, stabilising between 7 and 10 minutes after initiating hyperoxia, suggesting that oxygen diffusion primarily occurs via pial arteries and arteries at the base of the skull, both of which are in proximity to CSF-filled spaces. Over a timescale of 16 minutes, smaller T1 changes, only observed on the high-resolution T1 maps, occurred in the posterior lateral ventricles, where the choroid plexus is found, and the cisterna magna, possibly because of mixing effects with the adjacent basilar cisterns. Conclusions: This study provides insights into the structure of CSF and dynamics of blood-CSF oxygen exchange, including their regional dependence. Moreover, the methodology presented here could, in the future, offer a valuable tool for characterising the passive diffusion of oxygen across cerebral blood vessel walls (i.e., their oxygen permeability), thereby providing a potential marker of cerebrovascular integrity.

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