The effect of succinate on brain NADH/NAD+ redox state and high energy phosphate metabolism in acute traumatic brain injury

Matthew G. Stovell*, Marius O. Mada, Adel Helmy, T. Adrian Carpenter, Eric P. Thelin, Jiun Lin Yan, Mathew R. Guilfoyle, Ibrahim Jalloh, Duncan J. Howe, Peter Grice, Andrew Mason, Susan Giorgi-Coll, Clare N. Gallagher, Michael P. Murphy, David K. Menon, Peter J. Hutchinson, Keri L.H. Carpenter

*Corresponding author for this work

Research output: Contribution to journalJournal Article peer-review

41 Scopus citations

Abstract

A key pathophysiological process and therapeutic target in the critical early post-injury period of traumatic brain injury (TBI) is cell mitochondrial dysfunction; characterised by elevation of brain lactate/pyruvate (L/P) ratio in the absence of hypoxia. We previously showed that succinate can improve brain extracellular chemistry in acute TBI, but it was not clear if this translates to a change in downstream energy metabolism. We studied the effect of microdialysis-delivered succinate on brain energy state (phosphocreatine/ATP ratio (PCr/ATP)) with 31P MRS at 3T, and tissue NADH/NAD+ redox state using microdialysis (L/P ratio) in eight patients with acute major TBI (mean 7 days). Succinate perfusion was associated with increased extracellular pyruvate (+26%, p < 0.0001) and decreased L/P ratio (−13%, p < 0.0001) in patients overall (baseline-vs-supplementation over time), but no clear-cut change in 31P MRS PCr/ATP existed in our cohort (p > 0.4, supplemented-voxel-vs-contralateral voxel). However, the percentage decrease in L/P ratio for each patient following succinate perfusion correlated significantly with their percentage increase in PCr/ATP ratio (Spearman's rank correlation, r = −0.86, p = 0.024). Our findings support the interpretation that L/P ratio is linked to brain energy state, and that succinate may support brain energy metabolism in select TBI patients suffering from mitochondrial dysfunction.

Original languageEnglish
Article number11140
JournalScientific Reports
Volume8
Issue number1
DOIs
StatePublished - 01 12 2018

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© 2018, The Author(s).

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