Age-dependent white matter disruptions after military traumatic brain injury: Multivariate analysis results from ENIGMA brain injury

Heather C. Bouchard; Delin Sun; Emily L. Dennis; Mary R. Newsome; Seth G. Disner; Jeremy Elman; Annelise Silva; Carmen Velez; Andrei Irimia; Nicholas D. Davenport; Scott R. Sponheim; Carol E. Franz; William S. Kremen; Michael J. Coleman; M. Wright Williams; Elbert Geuze; Inga K. Koerte; Martha E. Shenton; Maheen M. Adamson; Raul Coimbra; Gerald Grant; Lori Shutter; Mark S. George; Ross D. Zafonte; Thomas W. McAllister; Murray B. Stein; Paul M. Thompson; Elisabeth A. Wilde; David F. Tate; Aristeidis Sotiras; Rajendra A. Morey

doi:10.1002/hbm.25811

Age-dependent white matter disruptions after military traumatic brain injury: Multivariate analysis results from ENIGMA brain injury

Heather C. Bouchard, Delin Sun, Emily L. Dennis, Mary R. Newsome, Seth G. Disner, Jeremy Elman, Annelise Silva, Carmen Velez, Andrei Irimia, Nicholas D. Davenport, Scott R. Sponheim, Carol E. Franz, William S. Kremen, Michael J. Coleman, M. Wright Williams, Elbert Geuze, Inga K. Koerte, Martha E. Shenton, Maheen M. Adamson, Raul CoimbraGerald Grant, Lori Shutter, Mark S. George, Ross D. Zafonte, Thomas W. McAllister, Murray B. Stein, Paul M. Thompson, Elisabeth A. Wilde, David F. Tate, Aristeidis Sotiras, Rajendra A. Morey

Research output: Contribution to journal › Article › peer-review

7 Scopus citations

Abstract

Mild Traumatic brain injury (mTBI) is a signature wound in military personnel, and repetitive mTBI has been linked to age-related neurogenerative disorders that affect white matter (WM) in the brain. However, findings of injury to specific WM tracts have been variable and inconsistent. This may be due to the heterogeneity of mechanisms, etiology, and comorbid disorders related to mTBI. Non-negative matrix factorization (NMF) is a data-driven approach that detects covarying patterns (components) within high-dimensional data. We applied NMF to diffusion imaging data from military Veterans with and without a self-reported TBI history. NMF identified 12 independent components derived from fractional anisotropy (FA) in a large dataset (n = 1,475) gathered through the ENIGMA (Enhancing Neuroimaging Genetics through Meta-Analysis) Military Brain Injury working group. Regressions were used to examine TBI- and mTBI-related associations in NMF-derived components while adjusting for age, sex, post-traumatic stress disorder, depression, and data acquisition site/scanner. We found significantly stronger age-dependent effects of lower FA in Veterans with TBI than Veterans without in four components (q < 0.05), which are spatially unconstrained by traditionally defined WM tracts. One component, occupying the most peripheral location, exhibited significantly stronger age-dependent differences in Veterans with mTBI. We found NMF to be powerful and effective in detecting covarying patterns of FA associated with mTBI by applying standard parametric regression modeling. Our results highlight patterns of WM alteration that are differentially affected by TBI and mTBI in younger compared to older military Veterans.

Original language	English
Pages (from-to)	2653-2667
Number of pages	15
Journal	Human Brain Mapping
Volume	43
Issue number	8
DOIs	https://doi.org/10.1002/hbm.25811
State	Published - Jun 1 2022

Keywords

ENIGMA
diffusion MRI
mTBI
military
nonnegative matrix factorization
traumatic brain injury

Access to Document

10.1002/hbm.25811

Cite this

Bouchard, H. C., Sun, D., Dennis, E. L., Newsome, M. R., Disner, S. G., Elman, J., Silva, A., Velez, C., Irimia, A., Davenport, N. D., Sponheim, S. R., Franz, C. E., Kremen, W. S., Coleman, M. J., Williams, M. W., Geuze, E., Koerte, I. K., Shenton, M. E., Adamson, M. M., ... Morey, R. A. (2022). Age-dependent white matter disruptions after military traumatic brain injury: Multivariate analysis results from ENIGMA brain injury. Human Brain Mapping, 43(8), 2653-2667. https://doi.org/10.1002/hbm.25811

@article{377785514a4c4f5eaae1d2b0bb47d4a5,

title = "Age-dependent white matter disruptions after military traumatic brain injury: Multivariate analysis results from ENIGMA brain injury",

abstract = "Mild Traumatic brain injury (mTBI) is a signature wound in military personnel, and repetitive mTBI has been linked to age-related neurogenerative disorders that affect white matter (WM) in the brain. However, findings of injury to specific WM tracts have been variable and inconsistent. This may be due to the heterogeneity of mechanisms, etiology, and comorbid disorders related to mTBI. Non-negative matrix factorization (NMF) is a data-driven approach that detects covarying patterns (components) within high-dimensional data. We applied NMF to diffusion imaging data from military Veterans with and without a self-reported TBI history. NMF identified 12 independent components derived from fractional anisotropy (FA) in a large dataset (n = 1,475) gathered through the ENIGMA (Enhancing Neuroimaging Genetics through Meta-Analysis) Military Brain Injury working group. Regressions were used to examine TBI- and mTBI-related associations in NMF-derived components while adjusting for age, sex, post-traumatic stress disorder, depression, and data acquisition site/scanner. We found significantly stronger age-dependent effects of lower FA in Veterans with TBI than Veterans without in four components (q < 0.05), which are spatially unconstrained by traditionally defined WM tracts. One component, occupying the most peripheral location, exhibited significantly stronger age-dependent differences in Veterans with mTBI. We found NMF to be powerful and effective in detecting covarying patterns of FA associated with mTBI by applying standard parametric regression modeling. Our results highlight patterns of WM alteration that are differentially affected by TBI and mTBI in younger compared to older military Veterans.",

keywords = "ENIGMA, diffusion MRI, mTBI, military, nonnegative matrix factorization, traumatic brain injury",

author = "Bouchard, {Heather C.} and Delin Sun and Dennis, {Emily L.} and Newsome, {Mary R.} and Disner, {Seth G.} and Jeremy Elman and Annelise Silva and Carmen Velez and Andrei Irimia and Davenport, {Nicholas D.} and Sponheim, {Scott R.} and Franz, {Carol E.} and Kremen, {William S.} and Coleman, {Michael J.} and Williams, {M. Wright} and Elbert Geuze and Koerte, {Inga K.} and Shenton, {Martha E.} and Adamson, {Maheen M.} and Raul Coimbra and Gerald Grant and Lori Shutter and George, {Mark S.} and Zafonte, {Ross D.} and McAllister, {Thomas W.} and Stein, {Murray B.} and Thompson, {Paul M.} and Wilde, {Elisabeth A.} and Tate, {David F.} and Aristeidis Sotiras and Morey, {Rajendra A.}",

note = "Publisher Copyright: {\textcopyright} 2022 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.",

year = "2022",

month = jun,

day = "1",

doi = "10.1002/hbm.25811",

language = "English",

volume = "43",

pages = "2653--2667",

journal = "Human Brain Mapping",

issn = "1065-9471",

number = "8",

}

Bouchard, HC, Sun, D, Dennis, EL, Newsome, MR, Disner, SG, Elman, J, Silva, A, Velez, C, Irimia, A, Davenport, ND, Sponheim, SR, Franz, CE, Kremen, WS, Coleman, MJ, Williams, MW, Geuze, E, Koerte, IK, Shenton, ME, Adamson, MM, Coimbra, R, Grant, G, Shutter, L, George, MS, Zafonte, RD, McAllister, TW, Stein, MB, Thompson, PM, Wilde, EA, Tate, DF, Sotiras, A & Morey, RA 2022, 'Age-dependent white matter disruptions after military traumatic brain injury: Multivariate analysis results from ENIGMA brain injury', Human Brain Mapping, vol. 43, no. 8, pp. 2653-2667. https://doi.org/10.1002/hbm.25811

TY - JOUR

T1 - Age-dependent white matter disruptions after military traumatic brain injury

T2 - Multivariate analysis results from ENIGMA brain injury

AU - Bouchard, Heather C.

AU - Sun, Delin

AU - Dennis, Emily L.

AU - Newsome, Mary R.

AU - Disner, Seth G.

AU - Elman, Jeremy

AU - Silva, Annelise

AU - Velez, Carmen

AU - Irimia, Andrei

AU - Davenport, Nicholas D.

AU - Sponheim, Scott R.

AU - Franz, Carol E.

AU - Kremen, William S.

AU - Coleman, Michael J.

AU - Williams, M. Wright

AU - Geuze, Elbert

AU - Koerte, Inga K.

AU - Shenton, Martha E.

AU - Adamson, Maheen M.

AU - Coimbra, Raul

AU - Grant, Gerald

AU - Shutter, Lori

AU - George, Mark S.

AU - Zafonte, Ross D.

AU - McAllister, Thomas W.

AU - Stein, Murray B.

AU - Thompson, Paul M.

AU - Wilde, Elisabeth A.

AU - Tate, David F.

AU - Sotiras, Aristeidis

AU - Morey, Rajendra A.

N1 - Publisher Copyright: © 2022 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

PY - 2022/6/1

Y1 - 2022/6/1

N2 - Mild Traumatic brain injury (mTBI) is a signature wound in military personnel, and repetitive mTBI has been linked to age-related neurogenerative disorders that affect white matter (WM) in the brain. However, findings of injury to specific WM tracts have been variable and inconsistent. This may be due to the heterogeneity of mechanisms, etiology, and comorbid disorders related to mTBI. Non-negative matrix factorization (NMF) is a data-driven approach that detects covarying patterns (components) within high-dimensional data. We applied NMF to diffusion imaging data from military Veterans with and without a self-reported TBI history. NMF identified 12 independent components derived from fractional anisotropy (FA) in a large dataset (n = 1,475) gathered through the ENIGMA (Enhancing Neuroimaging Genetics through Meta-Analysis) Military Brain Injury working group. Regressions were used to examine TBI- and mTBI-related associations in NMF-derived components while adjusting for age, sex, post-traumatic stress disorder, depression, and data acquisition site/scanner. We found significantly stronger age-dependent effects of lower FA in Veterans with TBI than Veterans without in four components (q < 0.05), which are spatially unconstrained by traditionally defined WM tracts. One component, occupying the most peripheral location, exhibited significantly stronger age-dependent differences in Veterans with mTBI. We found NMF to be powerful and effective in detecting covarying patterns of FA associated with mTBI by applying standard parametric regression modeling. Our results highlight patterns of WM alteration that are differentially affected by TBI and mTBI in younger compared to older military Veterans.

AB - Mild Traumatic brain injury (mTBI) is a signature wound in military personnel, and repetitive mTBI has been linked to age-related neurogenerative disorders that affect white matter (WM) in the brain. However, findings of injury to specific WM tracts have been variable and inconsistent. This may be due to the heterogeneity of mechanisms, etiology, and comorbid disorders related to mTBI. Non-negative matrix factorization (NMF) is a data-driven approach that detects covarying patterns (components) within high-dimensional data. We applied NMF to diffusion imaging data from military Veterans with and without a self-reported TBI history. NMF identified 12 independent components derived from fractional anisotropy (FA) in a large dataset (n = 1,475) gathered through the ENIGMA (Enhancing Neuroimaging Genetics through Meta-Analysis) Military Brain Injury working group. Regressions were used to examine TBI- and mTBI-related associations in NMF-derived components while adjusting for age, sex, post-traumatic stress disorder, depression, and data acquisition site/scanner. We found significantly stronger age-dependent effects of lower FA in Veterans with TBI than Veterans without in four components (q < 0.05), which are spatially unconstrained by traditionally defined WM tracts. One component, occupying the most peripheral location, exhibited significantly stronger age-dependent differences in Veterans with mTBI. We found NMF to be powerful and effective in detecting covarying patterns of FA associated with mTBI by applying standard parametric regression modeling. Our results highlight patterns of WM alteration that are differentially affected by TBI and mTBI in younger compared to older military Veterans.

KW - ENIGMA

KW - diffusion MRI

KW - mTBI

KW - military

KW - nonnegative matrix factorization

KW - traumatic brain injury

UR - http://www.scopus.com/inward/record.url?scp=85126249668&partnerID=8YFLogxK

U2 - 10.1002/hbm.25811

DO - 10.1002/hbm.25811

M3 - Article

C2 - 35289463

AN - SCOPUS:85126249668

SN - 1065-9471

VL - 43

SP - 2653

EP - 2667

JO - Human Brain Mapping

JF - Human Brain Mapping

IS - 8

ER -

Age-dependent white matter disruptions after military traumatic brain injury: Multivariate analysis results from ENIGMA brain injury

Abstract

Keywords

Access to Document

Other files and links

Fingerprint

Cite this