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Using dual-calibrated functional MRI to map brain oxygen supply and consumption in multiple sclerosis

Hannah L Chandler, Rachael C Stickland, Michael Germuska, Eleonora Patitucci, Catherine Foster, Shona Bhome-Dhaliwal, Thomas M Lancaster, Neeraj Saxena, Sharmila Khot, Valentina Tomassini, Richard G Wise
doi: https://doi.org/10.1101/2021.01.07.425819
Hannah L Chandler
1CUBRIC, School of Psychology, Cardiff University, Cardiff, United Kingdom
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Rachael C Stickland
2Department of Physical Therapy and Human Movement Sciences, Northwestern University, Chicago, IL, USA
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Michael Germuska
1CUBRIC, School of Psychology, Cardiff University, Cardiff, United Kingdom
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Eleonora Patitucci
1CUBRIC, School of Psychology, Cardiff University, Cardiff, United Kingdom
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Catherine Foster
3Wales Institute of Social and Economic Research and Data, Cardiff University, Cardiff
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Shona Bhome-Dhaliwal
4Cardiff University School of Medicine, Cardiff
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Thomas M Lancaster
1CUBRIC, School of Psychology, Cardiff University, Cardiff, United Kingdom
5Department of Psychology, University of Bath, Bath, UK
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Neeraj Saxena
1CUBRIC, School of Psychology, Cardiff University, Cardiff, United Kingdom
6Department of Anaesthetics, Intensive Care and Pain Medicine, Cwm Taf Morgannwg, University Health Board, Abercynon, UK
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Sharmila Khot
1CUBRIC, School of Psychology, Cardiff University, Cardiff, United Kingdom
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Valentina Tomassini
7Institute for Advanced Biomedical Technologies, Department of Neuroscience, Imaging and Clinical Sciences, University G. d’Annunzio of Chieti-Pescara, Chieti, Italy
8MS Centre, Neurology Unit, “SS. Annunziata” University Hospital, Chieti, Italy
9Division of Psychological Medicine and Clinical Neurosciences, School of Medicine, Cardiff University, Cardiff, UK
10Helen Durham Centre for Neuroinflammation, University Hospital of Wales, Cardiff, UK
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Richard G Wise
1CUBRIC, School of Psychology, Cardiff University, Cardiff, United Kingdom
7Institute for Advanced Biomedical Technologies, Department of Neuroscience, Imaging and Clinical Sciences, University G. d’Annunzio of Chieti-Pescara, Chieti, Italy
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  • For correspondence: richard.wise@unich.it
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Abstract

Evidence suggests that cerebrovascular function and oxygen consumption are altered in multiple sclerosis (MS). Here, we quantified the vascular and oxygen metabolic MRI burden in patients with MS (PwMS) and assessed the relationship between these MRI measures of and metrics of damage and disability. In PwMS and in matched healthy volunteers, we applied a newly developed dual-calibrated fMRI method of acquisition and analysis to map grey matter (GM) cerebral blood flow (CBF), oxygen extraction fraction (OEF), cerebral metabolic rate of oxygen consumption (CMRO2) and effective oxygen diffusivity of the capillary network (DC). We also quantified physical and cognitive function in PwMS and controls. There was no significant difference in GM volume between 22 PwMS and 20 healthy controls (p=0.302). Significant differences in CBF (PwMS vs. controls: 44.91 ± 6.10 vs. 48.90 ± 5.87 ml/100g/min, p=0.010), CMRO2 (117.69 ± 17.31 vs. 136.49 ± 14.48 μmol/100g/min p<0.001) and DC (2.70 ± 0.51 vs. 3.18 ± 0.41 μmol/100g/mmHg/min, p=0.002) were observed in the PwMS. No significant between-group differences were observed for OEF (PwMS vs. controls: 0.38 ± 0.09 vs. 0.39 ± 0.02, p=0.358). Regional analysis showed widespread reductions in CMRO2 and DC for PwMS compared to healthy volunteers. There was a significant correlation between physiological measures and T2 lesion volume, but no association with current clinical disability. Our findings demonstrate concurrent reductions in oxygen supply and consumption in the absence of an alteration in oxygen extraction that may be indicative of a reduced demand for oxygen (O2), an impaired transfer of O2 from capillaries to mitochondria, and/or a reduced ability to utilise O2 that is available at the mitochondria. With no between-group differences in GM volume, our results suggest that changes in brain physiology may precede MRI-detectable GM loss and thus may be one of the pathological drivers of neurodegeneration and disease progression.

Competing Interest Statement

The authors have declared no competing interest.

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Posted January 08, 2021.
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Using dual-calibrated functional MRI to map brain oxygen supply and consumption in multiple sclerosis
Hannah L Chandler, Rachael C Stickland, Michael Germuska, Eleonora Patitucci, Catherine Foster, Shona Bhome-Dhaliwal, Thomas M Lancaster, Neeraj Saxena, Sharmila Khot, Valentina Tomassini, Richard G Wise
bioRxiv 2021.01.07.425819; doi: https://doi.org/10.1101/2021.01.07.425819
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Using dual-calibrated functional MRI to map brain oxygen supply and consumption in multiple sclerosis
Hannah L Chandler, Rachael C Stickland, Michael Germuska, Eleonora Patitucci, Catherine Foster, Shona Bhome-Dhaliwal, Thomas M Lancaster, Neeraj Saxena, Sharmila Khot, Valentina Tomassini, Richard G Wise
bioRxiv 2021.01.07.425819; doi: https://doi.org/10.1101/2021.01.07.425819

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