Group-Wise Evaluation and Comparison of White Matter Fiber Strain and Maximum Principal Strain in Sports-Related Concussion

Sports-related concussion is a major public health problem in the United States and yet its biomechanical mechanisms remain unclear. In vitro studies demonstrate axonal elongation as a potential injury mechanism; however, current response-based injury predictors (e.g., maximum principal strain, ε(ep...

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Bibliographic Details
Published inJournal of neurotrauma Vol. 32; no. 7; pp. 441 - 454
Main Authors Ji, Songbai, Zhao, Wei, Ford, James C., Beckwith, Jonathan G., Bolander, Richard P., Greenwald, Richard M., Flashman, Laura A., Paulsen, Keith D., McAllister, Thomas W.
Format Journal Article
LanguageEnglish
Published United States Mary Ann Liebert, Inc 01.04.2015
Subjects
Adolescent
Athletic Injuries - complications
Athletic Injuries - pathology
Brain
Brain Concussion - etiology
Brain Concussion - pathology
Concussion
Diffuse Axonal Injury - etiology
Diffuse Axonal Injury - pathology
Diffusion Tensor Imaging
Female
Fibers
Humans
Male
Nerve Fibers, Myelinated - pathology
Original
Sports injuries
Strain
White Matter - pathology
Young Adult
traumatic brain injury
diffusion tensor imaging
axonal injury
finite element method
models of injury
Online AccessGet full text
ISSN0897-7151
1557-9042
1557-9042
DOI10.1089/neu.2013.3268

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Abstract Sports-related concussion is a major public health problem in the United States and yet its biomechanical mechanisms remain unclear. In vitro studies demonstrate axonal elongation as a potential injury mechanism; however, current response-based injury predictors (e.g., maximum principal strain, ε(ep)) typically do not incorporate axonal orientations. We investigated the significance of white matter (WM) fiber orientation in strain estimation and compared fiber strain (ε(n)) with ε(ep) for 11 athletes with a clinical diagnosis of concussion. Geometrically accurate subject-specific head models with high mesh quality were created based on the Dartmouth Head Injury Model (DHIM), which was successfully validated (performance categorized as "good" to "excellent"). For WM regions estimated to be exposed to high strains using a range of injury thresholds (0.09-0.28), substantial differences existed between ε(n) and ε(ep) in both distribution (Dice coefficient of 0.13-0.33) and extent (∼ 5-10-fold differences), especially at higher threshold levels and higher rotational acceleration magnitudes. For example, an average of 3.2% vs. 29.8% of WM was predicted above an optimal threshold of 0.18 established from an in vivo animal study using ε(n) and ε(ep), respectively, with an average Dice coefficient of 0.14. The distribution of WM regions with high ε(n) was consistent with typical heterogeneous patterns of WM disruptions in diffuse axonal injury, and the group-wise extent at the optimal threshold matched well with the percentage of WM voxels experiencing significant longitudinal changes of fractional anisotropy and mean diffusivity (3.2% and 3.44%, respectively) found from a separate independent study. These results suggest the significance of incorporating WM microstructural anisotropy in future brain injury studies.
AbstractList Sports-related concussion is a major public health problem in the United States and yet its biomechanical mechanisms remain unclear. In vitro studies demonstrate axonal elongation as a potential injury mechanism; however, current response-based injury predictors (e.g., maximum principal strain, [Formula omitted; see PDF] ) typically do not incorporate axonal orientations. We investigated the significance of white matter (WM) fiber orientation in strain estimation and compared fiber strain ( [Formula omitted; see PDF] ) with [Formula omitted; see PDF] for 11 athletes with a clinical diagnosis of concussion. Geometrically accurate subject-specific head models with high mesh quality were created based on the Dartmouth Head Injury Model (DHIM), which was successfully validated (performance categorized as "good" to "excellent"). For WM regions estimated to be exposed to high strains using a range of injury thresholds (0.09-0.28), substantial differences existed between [Formula omitted; see PDF] and [Formula omitted; see PDF] in both distribution (Dice coefficient of 0.13-0.33) and extent (∼5-10-fold differences), especially at higher threshold levels and higher rotational acceleration magnitudes. For example, an average of 3.2% vs. 29.8% of WM was predicted above an optimal threshold of 0.18 established from an in vivo animal study using [Formula omitted; see PDF] and [Formula omitted; see PDF], respectively, with an average Dice coefficient of 0.14. The distribution of WM regions with high [Formula omitted; see PDF] was consistent with typical heterogeneous patterns of WM disruptions in diffuse axonal injury, and the group-wise extent at the optimal threshold matched well with the percentage of WM voxels experiencing significant longitudinal changes of fractional anisotropy and mean diffusivity (3.2% and 3.44%, respectively) found from a separate independent study. These results suggest the significance of incorporating WM microstructural anisotropy in future brain injury studies.
Sports-related concussion is a major public health problem in the United States and yet its biomechanical mechanisms remain unclear. In vitro studies demonstrate axonal elongation as a potential injury mechanism; however, current response-based injury predictors (e.g., maximum principal strain, ε(ep)) typically do not incorporate axonal orientations. We investigated the significance of white matter (WM) fiber orientation in strain estimation and compared fiber strain (ε(n)) with ε(ep) for 11 athletes with a clinical diagnosis of concussion. Geometrically accurate subject-specific head models with high mesh quality were created based on the Dartmouth Head Injury Model (DHIM), which was successfully validated (performance categorized as "good" to "excellent"). For WM regions estimated to be exposed to high strains using a range of injury thresholds (0.09-0.28), substantial differences existed between ε(n) and ε(ep) in both distribution (Dice coefficient of 0.13-0.33) and extent (∼ 5-10-fold differences), especially at higher threshold levels and higher rotational acceleration magnitudes. For example, an average of 3.2% vs. 29.8% of WM was predicted above an optimal threshold of 0.18 established from an in vivo animal study using ε(n) and ε(ep), respectively, with an average Dice coefficient of 0.14. The distribution of WM regions with high ε(n) was consistent with typical heterogeneous patterns of WM disruptions in diffuse axonal injury, and the group-wise extent at the optimal threshold matched well with the percentage of WM voxels experiencing significant longitudinal changes of fractional anisotropy and mean diffusivity (3.2% and 3.44%, respectively) found from a separate independent study. These results suggest the significance of incorporating WM microstructural anisotropy in future brain injury studies.
Sports-related concussion is a major public health problem in the United States and yet its biomechanical mechanisms remain unclear. In vitro studies demonstrate axonal elongation as a potential injury mechanism; however, current response-based injury predictors (e.g., maximum principal strain, \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_{ep}$$ \end{document} ) typically do not incorporate axonal orientations. We investigated the significance of white matter (WM) fiber orientation in strain estimation and compared fiber strain ( \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_n$$ \end{document} ) with \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_{ep}$$ \end{document} for 11 athletes with a clinical diagnosis of concussion. Geometrically accurate subject-specific head models with high mesh quality were created based on the Dartmouth Head Injury Model (DHIM), which was successfully validated (performance categorized as “good” to “excellent”). For WM regions estimated to be exposed to high strains using a range of injury thresholds (0.09–0.28), substantial differences existed between \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_n$$ \end{document} and \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_{ep}$$ \end{document} in both distribution (Dice coefficient of 0.13–0.33) and extent (∼5–10-fold differences), especially at higher threshold levels and higher rotational acceleration magnitudes. For example, an average of 3.2% vs. 29.8% of WM was predicted above an optimal threshold of 0.18 established from an in vivo animal study using \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_n$$ \end{document} and \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_{ep}$$ \end{document} , respectively, with an average Dice coefficient of 0.14. The distribution of WM regions with high \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_n$$ \end{document} was consistent with typical heterogeneous patterns of WM disruptions in diffuse axonal injury, and the group-wise extent at the optimal threshold matched well with the percentage of WM voxels experiencing significant longitudinal changes of fractional anisotropy and mean diffusivity (3.2% and 3.44%, respectively) found from a separate independent study. These results suggest the significance of incorporating WM microstructural anisotropy in future brain injury studies.
Sports-related concussion is a major public health problem in the United States and yet its biomechanical mechanisms remain unclear. In vitro studies demonstrate axonal elongation as a potential injury mechanism; however, current response-based injury predictors (e.g., maximum principal strain, \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\use p ackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pif o n t}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_{ep}$$ \end{document}) typically do not incorporate axonal orientations. We investigated the significance of white matter (WM) fiber orientation in strain estimation and compared fiber strain (\documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\us e package{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pi f o nt}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_n$$ \end{document}) with \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\use p ackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pif o n t}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_{ep}$$ \end{document} for 11 athletes with a clinical diagnosis of concussion. Geometrically accurate subject-specific head models with high mesh quality were created based on the Dartmouth Head Injury Model (DHIM), which was successfully validated (performance categorized as "good" to "excellent"). For WM regions estimated to be exposed to high strains using a range of injury thresholds (0.09-0.28), substantial differences existed between \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\use p ackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pif o n t}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_n$$ \end{document} and \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\use p ackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pif o n t}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_{ep}$$ \end{document} in both distribution (Dice coefficient of 0.13-0.33) and extent (5-10-fold differences), especially at higher threshold levels and higher rotational acceleration magnitudes. For example, an average of 3.2% vs. 29.8% of WM was predicted above an optimal threshold of 0.18 established from an in vivo animal study using \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\use p ackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pif o n t}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_n$$ \end{document} and \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\use p ackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pif o n t}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_{ep}$$ \end{document}, respectively, with an average Dice coefficient of 0.14. The distribution of WM regions with high \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\use p ackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pif o n t}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes {10} {9} {7} {6} \begin{document} $$\varepsilon_n$$ \end{document} was consistent with typical heterogeneous patterns of WM disruptions in diffuse axonal injury, and the group-wise extent at the optimal threshold matched well with the percentage of WM voxels experiencing significant longitudinal changes of fractional anisotropy and mean diffusivity (3.2% and 3.44%, respectively) found from a separate independent study. These results suggest the significance of incorporating WM microstructural anisotropy in future brain injury studies.
Sports-related concussion is a major public health problem in the United States and yet its biomechanical mechanisms remain unclear. In vitro studies demonstrate axonal elongation as a potential injury mechanism; however, current response-based injury predictors (e.g., maximum principal strain, ε(ep)) typically do not incorporate axonal orientations. We investigated the significance of white matter (WM) fiber orientation in strain estimation and compared fiber strain (ε(n)) with ε(ep) for 11 athletes with a clinical diagnosis of concussion. Geometrically accurate subject-specific head models with high mesh quality were created based on the Dartmouth Head Injury Model (DHIM), which was successfully validated (performance categorized as "good" to "excellent"). For WM regions estimated to be exposed to high strains using a range of injury thresholds (0.09-0.28), substantial differences existed between ε(n) and ε(ep) in both distribution (Dice coefficient of 0.13-0.33) and extent (∼ 5-10-fold differences), especially at higher threshold levels and higher rotational acceleration magnitudes. For example, an average of 3.2% vs. 29.8% of WM was predicted above an optimal threshold of 0.18 established from an in vivo animal study using ε(n) and ε(ep), respectively, with an average Dice coefficient of 0.14. The distribution of WM regions with high ε(n) was consistent with typical heterogeneous patterns of WM disruptions in diffuse axonal injury, and the group-wise extent at the optimal threshold matched well with the percentage of WM voxels experiencing significant longitudinal changes of fractional anisotropy and mean diffusivity (3.2% and 3.44%, respectively) found from a separate independent study. These results suggest the significance of incorporating WM microstructural anisotropy in future brain injury studies.Sports-related concussion is a major public health problem in the United States and yet its biomechanical mechanisms remain unclear. In vitro studies demonstrate axonal elongation as a potential injury mechanism; however, current response-based injury predictors (e.g., maximum principal strain, ε(ep)) typically do not incorporate axonal orientations. We investigated the significance of white matter (WM) fiber orientation in strain estimation and compared fiber strain (ε(n)) with ε(ep) for 11 athletes with a clinical diagnosis of concussion. Geometrically accurate subject-specific head models with high mesh quality were created based on the Dartmouth Head Injury Model (DHIM), which was successfully validated (performance categorized as "good" to "excellent"). For WM regions estimated to be exposed to high strains using a range of injury thresholds (0.09-0.28), substantial differences existed between ε(n) and ε(ep) in both distribution (Dice coefficient of 0.13-0.33) and extent (∼ 5-10-fold differences), especially at higher threshold levels and higher rotational acceleration magnitudes. For example, an average of 3.2% vs. 29.8% of WM was predicted above an optimal threshold of 0.18 established from an in vivo animal study using ε(n) and ε(ep), respectively, with an average Dice coefficient of 0.14. The distribution of WM regions with high ε(n) was consistent with typical heterogeneous patterns of WM disruptions in diffuse axonal injury, and the group-wise extent at the optimal threshold matched well with the percentage of WM voxels experiencing significant longitudinal changes of fractional anisotropy and mean diffusivity (3.2% and 3.44%, respectively) found from a separate independent study. These results suggest the significance of incorporating WM microstructural anisotropy in future brain injury studies.
Author Zhao, Wei
Ji, Songbai
Greenwald, Richard M.
Flashman, Laura A.
Beckwith, Jonathan G.
Bolander, Richard P.
Paulsen, Keith D.
Ford, James C.
McAllister, Thomas W.
Author_xml – sequence: 1
  givenname: Songbai
  surname: Ji
  fullname: Ji, Songbai
  organization: Thayer School of Engineering, Dartmouth College, Hanover, New Hampshire., Department of Surgery and Orthopedic Surgery, Geisel School of Medicine at Dartmouth, Lebanon, New Hampshire
– sequence: 2
  givenname: Wei
  surname: Zhao
  fullname: Zhao, Wei
  organization: Thayer School of Engineering, Dartmouth College, Hanover, New Hampshire
– sequence: 3
  givenname: James C.
  surname: Ford
  fullname: Ford, James C.
  organization: Department of Psychiatry, Geisel School of Medicine at Dartmouth, Lebanon, New Hampshire
– sequence: 4
  givenname: Jonathan G.
  surname: Beckwith
  fullname: Beckwith, Jonathan G.
  organization: Simbex, Lebanon, New Hampshire
– sequence: 5
  givenname: Richard P.
  surname: Bolander
  fullname: Bolander, Richard P.
  organization: Simbex, Lebanon, New Hampshire
– sequence: 6
  givenname: Richard M.
  surname: Greenwald
  fullname: Greenwald, Richard M.
  organization: Thayer School of Engineering, Dartmouth College, Hanover, New Hampshire., Simbex, Lebanon, New Hampshire
– sequence: 7
  givenname: Laura A.
  surname: Flashman
  fullname: Flashman, Laura A.
  organization: Department of Psychiatry, Geisel School of Medicine at Dartmouth, Lebanon, New Hampshire
– sequence: 8
  givenname: Keith D.
  surname: Paulsen
  fullname: Paulsen, Keith D.
  organization: Thayer School of Engineering, Dartmouth College, Hanover, New Hampshire
– sequence: 9
  givenname: Thomas W.
  surname: McAllister
  fullname: McAllister, Thomas W.
  organization: Department of Psychiatry, Indiana University School of Medicine, Indianapolis, Indiana
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24735430$$D View this record in MEDLINE/PubMed
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diffusion tensor imaging
axonal injury
finite element method
models of injury
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Snippet Sports-related concussion is a major public health problem in the United States and yet its biomechanical mechanisms remain unclear. In vitro studies...
Sports-related concussion is a major public health problem in the United States and yet its biomechanical mechanisms remain unclear. In vitro studies...
SourceID pubmedcentral
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pubmed
crossref
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage 441
SubjectTerms Adolescent
Athletic Injuries - complications
Athletic Injuries - pathology
Brain
Brain Concussion - etiology
Brain Concussion - pathology
Concussion
Diffuse Axonal Injury - etiology
Diffuse Axonal Injury - pathology
Diffusion Tensor Imaging
Female
Fibers
Humans
Male
Nerve Fibers, Myelinated - pathology
Original
Sports injuries
Strain
White Matter - pathology
Young Adult
Title Group-Wise Evaluation and Comparison of White Matter Fiber Strain and Maximum Principal Strain in Sports-Related Concussion
URI https://www.ncbi.nlm.nih.gov/pubmed/24735430
https://www.proquest.com/docview/1666335672
https://www.proquest.com/docview/1667350505
https://www.proquest.com/docview/1837294772
https://pubmed.ncbi.nlm.nih.gov/PMC4376290
Volume 32
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