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Regional glucose metabolic decreases with ageing are associated with microstructural white matter changes: a simultaneous PET/MR study

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Abstract

Purpose

Human ageing is associated with a regional reduction in cerebral neuronal activity as assessed by numerous studies on brain glucose metabolism and perfusion, grey matter (GM) density and white matter (WM) integrity. As glucose metabolism may impact energetics to maintain myelin integrity, but changes in functional connectivity may also alter regional metabolism, we conducted a cross-sectional simultaneous FDG PET/MR study in a large cohort of healthy volunteers with a wide age range, to directly assess the underlying associations between reduced glucose metabolism, GM atrophy and decreased WM integrity in a single ageing cohort.

Methods

In 94 healthy subjects between 19.9 and 82.5 years (mean 50.1 ± 17.1; 47 M/47F, MMSE ≥ 28), simultaneous FDG-PET, structural MR and diffusion tensor imaging (DTI) were performed. Voxel-wise associations between age and grey matter (GM) density, RBV partial-volume corrected (PVC) glucose metabolism, white matter (WM) fractional anisotropy (FA) and mean diffusivity (MD), and age were assessed. Clusters representing changes in glucose metabolism correlating significantly with ageing were used as seed regions for tractography. Both linear and quadratic ageing models were investigated.

Results

An expected age-related reduction in GM density was observed bilaterally in the frontal, lateral and medial temporal cortex, striatum and cerebellum. After PVC, relative FDG uptake was negatively correlated with age in the inferior and midfrontal, cingulate and parietal cortex and subcortical regions, bilaterally. FA decreased with age throughout the entire brain WM. Four white matter tracts were identified connecting brain regions with declining glucose metabolism with age. Within these, relative FDG uptake in both origin and target clusters correlated positively with FA (0.32 ≤ r ≤ 0.71) and negatively with MD (− 0.75 ≤ r ≤  − 0.41).

Conclusion

After appropriate PVC, we demonstrated that regional cerebral glucose metabolic declines with age and that these changes are related to microstructural changes in the interconnecting WM tracts. The temporal course and potential causality between ageing effects on glucose metabolism and WM integrity should be further investigated in longitudinal cohort PET/MR studies.

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Abbreviations

GM:

Grey matter

WM:

White matter

FDG:

Fluorodeoxyglucose

PET/MR:

Positron emission tomography/magnetic resonance

DTI:

Diffusion tensor imaging

MRI:

Magnetic resonance imaging

FA:

Fractional anisotropy

PVC:

Partial volume correction

MD:

Mean diffusivity

SPM:

Statistical parametric mapping

WMH:

White matter hyperintensities

SPECT:

Single photon emission computed tomography

CBF:

Cerebral blood flow

ASL:

Arterial spin labelling

CSF:

Cerebrospinal fluid

GTM:

Geometric transfer matrix

VOI:

Volume-of-interest

ROI:

Region of interest

MMSE:

Mini-mental state examination

BDI:

Beck’s depression inventory

TOF:

Time of flight

OSEM:

Ordered subset expectation maximization

FWHM:

Full width half maximum

TR:

Repetition time

TE:

Echo time

FLAIR:

Fluid-attenuated inversion recovery

VBM:

Voxel-based morphometry

TIV:

Total intra-cranial volume

FWE:

Family wise error

kE :

Cluster extent

RPD:

Reduction per decade

RBV:

Region-based voxel-wise

FSL:

FMRIB software library

BIC:

Bayesian information criterion

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Acknowledgements

The authors acknowledge the contributions by Stefanie Willekens, PhD, on data acquisition, Kim Serdons, Pharm PhD and the radiopharmacy team for tracer production, Kwinten Porters, Jef Van Loock, Guido Putzeys, Kris Byloos and Stefan Ghysels for data acquisition, and Ronald Peeters, Nathalie Mertens from the PET/MR physics team.

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Authors and Affiliations

  1. Nuclear Medicine and Molecular Imaging, Department of Imaging and Pathology, KU Leuven, Leuven, Belgium

    June van Aalst, Martijn Devrome, Donatienne Van Weehaeghe, Ahmadreza Rezaei, Georg Schramm, Jenny Ceccarini, Michel Koole & Koen Van Laere

  2. Division of Nuclear Medicine, University Hospitals Leuven, Leuven, Belgium

    Donatienne Van Weehaeghe & Koen Van Laere

  3. Translational MRI, Department of Imaging and Pathology, KU Leuven, Leuven, Belgium

    Ahmed Radwan & Stefan Sunaert

  4. Radiology, University Hospitals Leuven, Leuven, Belgium

    Stefan Sunaert

  5. UZ Leuven, Campus Gasthuisberg, Nucleaire Geneeskunde, E901, Herestraat 49, BE-3000 , Leuven, Belgium

    Koen Van Laere

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  1. June van Aalst
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van Aalst, J., Devrome, M., Van Weehaeghe, D. et al. Regional glucose metabolic decreases with ageing are associated with microstructural white matter changes: a simultaneous PET/MR study. Eur J Nucl Med Mol Imaging 49, 664–680 (2022). https://doi.org/10.1007/s00259-021-05518-6

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