Mild traumatic brain injury history is associated with lower brain network resilience in soldiers

Jacob R Powell; Joseph B Hopfinger; Kelly S Giovanello; Samuel R Walton; Stephen M DeLellis; Shawn F Kane; Gary E Means; Jason P Mihalik

doi:10.1093/braincomms/fcad201

journal article Open Access Jan 01, 2023

Mild traumatic brain injury history is associated with lower brain network resilience in soldiers

Jacob R Powell

Joseph B Hopfinger Kelly S Giovanello Samuel R Walton Stephen M DeLellis Shawn F Kane Gary E Means Jason P Mihalik

Brain Communications Vol. 5 No. 4 · Oxford University Press (OUP)

View at Publisher Save 10.1093/braincomms/fcad201

Abstract

AbstractSpecial Operations Forces combat soldiers sustain frequent blast and blunt neurotrauma, most often classified as mild traumatic brain injuries. Exposure to repetitive mild traumatic brain injuries is associated with persistent behavioural, cognitive, emotional and neurological symptoms later in life. Identifying neurophysiological changes associated with mild traumatic brain injury exposure, in the absence of present-day symptoms, is necessary for detecting future neurological risk. Advancements in graph theory and functional MRI have offered novel ways to analyse complex whole-brain network connectivity. Our purpose was to determine how mild traumatic brain injury history, lifetime incidence and recency affected whole-brain graph theoretical outcome measures. Healthy male Special Operations Forces combat soldiers (age = 33.2 ± 4.3 years) underwent multimodal neuroimaging at a biomedical research imaging centre using 3T Siemens Prisma or Biograph MRI scanners in this cross-sectional study. Anatomical and functional scans were preprocessed. The blood-oxygen-level-dependent signal was extracted from each functional MRI time series using the Big Brain 300 atlas. Correlations between atlas regions were calculated and Fisher z-transformed to generate subject-level correlation matrices. The Brain Connectivity Toolbox was used to obtain functional network measures for global efficiency (the average inverse shortest path length), local efficiency (the average global efficiency of each node and its neighbours), and assortativity coefficient (the correlation coefficient between the degrees of all nodes on two opposite ends of a link). General linear models were fit to compare mild traumatic brain injury lifetime incidence and recency. Nonparametric ANOVAs were used for tests on non-normally distributed data. Soldiers with a history of mild traumatic brain injury had significantly lower assortativity than those who did not self-report mild traumatic brain injury (t148 = 2.44, P = 0.016). The assortativity coefficient was significantly predicted by continuous mild traumatic brain injury lifetime incidence [F1,144 = 6.51, P = 0.012]. No differences were observed between recency groups, and no global or local efficiency differences were observed between mild traumatic brain injury history and lifetime incidence groups. Brain networks with greater assortativity have more resilient, interconnected hubs, while those with lower assortativity indicate widely distributed, vulnerable hubs. Greater lifetime mild traumatic brain injury incidence predicted lower assortativity in our study sample. Less resilient brain networks may represent a lack of physiological recovery in mild traumatic brain injury patients, who otherwise demonstrate clinical recovery, more vulnerability to future brain injury and increased risk for accelerated age-related neurodegenerative changes. Future longitudinal studies should investigate whether decreased brain network resilience may be a predictor for long-term neurological dysfunction.

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Details

Published: Jan 01, 2023
Vol/Issue: 5(4)
License: View

Authors

J

Jacob R Powell

Matthew Gfeller Center, Department of Exercise and Sport Science, University of North Carolina at Chapel Hill , Chapel Hill, NC 27599 , USA

J

Joseph B Hopfinger

Department of Psychology and Neuroscience, University of North Carolina at Chapel Hill , Chapel Hill, NC 27599 , USA

K

Kelly S Giovanello

Department of Psychology and Neuroscience, University of North Carolina at Chapel Hill , Chapel Hill, NC 27599 , USA

S

Samuel R Walton

Physical Medicine and Rehabilitation, School of Medicine, Virginia Commonwealth University , Richmond, VA 23284 , USA

S

Stephen M DeLellis

Fort Liberty Research Institute, The Geneva Foundation , Tacoma, WA 98402 , USA

S

Shawn F Kane

Matthew Gfeller Center, Department of Exercise and Sport Science, University of North Carolina at Chapel Hill , Chapel Hill, NC 27599 , USA; Department of Family Medicine, University of North Carolina at Chapel Hill , Chapel Hill, NC 27599 , USA

G

Gary E Means

United States Army Special Operations Command , Fort Liberty, NC 28303 , USA

J

Jason P Mihalik

Matthew Gfeller Center, Department of Exercise and Sport Science, University of North Carolina at Chapel Hill , Chapel Hill, NC 27599 , USA

Funding

University of North Carolina at Chapel Hill

Cite This Article

Jacob R Powell, Joseph B Hopfinger, Kelly S Giovanello, et al. (2023). Mild traumatic brain injury history is associated with lower brain network resilience in soldiers. Brain Communications, 5(4). https://doi.org/10.1093/braincomms/fcad201

Mild traumatic brain injury history is associated with lower brain network resilience in soldiers

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