Phosphate Brain Energy Metabolism and Cognition in Alzheimer’s Disease: A Spectroscopy
      Study Using Whole-Brain Volume-Coil 
      <sup>31</sup>Phosphorus Magnetic Resonance Spectroscopy at 7Tesla

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Abstract

Introduction

Mitochondrial dysfunction is a neurometabolic hallmark signaling abnormal brain energy metabolism (BEM) targeted as a potential early marker of Alzheimer’s disease (AD). Advanced imaging technologies, such as ³¹phosphorus magnetic resonance spectroscopy ( ³¹P MRS) at ultra-high-field (UHF) magnetic strength 7T, provide sensitive phosphate-BEM (p-BEM) data with precision. The study’s first goal was to develop a methodology to measure phosphate energy and membrane metabolites simultaneously across the whole-brain using volume-coil ³¹P MRS at 7T in three groups-cognitively normal (CN), amnestic mild cognitive impairment (aMCI), and AD. The second aim investigated whether p-BEM markers in the four brain regions-frontal, temporal, parietal, and occipital were significantly different across the three groups. The final goal examined correspondence between the p-BEM markers and cognition in the three groups.

Methods

Forty-one participants (CN = 15, aMCI = 15, AD = 11) were enrolled and completed cognitive assessment and scan. The cognitive domains included executive function (EF), memory, attention, visuospatial skills, and language. The p-BEM markers were measured using energy reserve index (PCr/t-ATP), energy consumption index (intracellular_Pi/t-ATP), metabolic state indicator (intracellular_Pi/PCr), and regulatory co-factors [magnesium (Mg ²⁺) and intracellular pH].

Results

Thirteen metabolites were measured simultaneously from the whole brain for all three group with high spectral resolution at UHF. In the aMCI group, a lower p-BEM was observed compared to CN group based on two markers, i.e., energy reserve (p = 0.009) and energy consumption ( p = 0.05) indices; whereas in AD a significant increase was found in metabolic stress indicator ( p = 0.007) and lower Mg ²⁺ ( p = 0.004) in the temporal lobes compared to aMCI using ANOVA between group analytical approach. Finally, using a linear mixed model, a significant positive correlation was found between Mg ²⁺ and cognitive performance of memory ( p = 0.013), EF ( p = 0.023), and attention ( p = 0.0003) in CN but not in aMCI or AD.

Conclusion

To our knowledge, this is the first study to show that it is possible to measure p-BEM in vivo with precision at UHF across the three groups. Moreover, the findings suggest that p-BEM may be compromised in aMCI even before an AD diagnosis, which in future studies should explore to examine whether this energy crisis contributes to some of the earliest neuropathophysiologic changes in AD.

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Author and article information

Contributors

Namrata Das: URI : http://loop.frontiersin.org/people/623334/overview

Jimin Ren: URI : http://loop.frontiersin.org/people/423952/overview

Jeffrey Spence: URI : http://loop.frontiersin.org/people/179895/overview

Sandra Bond Chapman: URI : http://loop.frontiersin.org/people/14898/overview

Journal

Journal ID (nlm-ta): Front Neurosci

Journal ID (iso-abbrev): Front Neurosci

Journal ID (publisher-id): Front. Neurosci.

Title: Frontiers in Neuroscience

Publisher: Frontiers Media S.A.

ISSN (Print): 1662-4548

ISSN (Electronic): 1662-453X

Publication date (Electronic): 06 April 2021

Publication date Collection: 2021

Volume: 15

Electronic Location Identifier: 641739

Affiliations

[1] ¹Center for BrainHealth, The University of Texas at Dallas , Dallas, TX, United States

[2] ²Department of Radiology, Advanced Imaging Research Center, University of Texas Southwestern Medical Center , Dallas, TX, United States

Author notes

Edited by: Lionel Carneiro, The Ohio State University, United States

Reviewed by: Anne-Karine Bouzier-Sore, Centre National de la Recherche Scientifique (CNRS), France; Jianping Jia, Capital Medical University, China

*Correspondence: Namrata Das, Namrata.Das@ 123456utdallas.edu

This article was submitted to Neuroenergetics, Nutrition and Brain Health, a section of the journal Frontiers in Neuroscience

Article

DOI: 10.3389/fnins.2021.641739

PMC ID: 8055842

PubMed ID: 33889067

SO-VID: 77968779-bb2f-4e78-ac67-234675b703d5

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 14 December 2020

Date accepted : 15 February 2021

Page count

Figures: 4, Tables: 5, Equations: 1, References: 46, Pages: 16, Words: 0

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