The influence of anisotropy on brain injury prediction

Giordano, Chiara; Cloots, R. J. H.; Dommelen, J.A.W. van; Kleiven, Svein

doi:10.1016/j.jbiomech.2013.12.036

Cited by 93 publications

(84 citation statements)

References 20 publications

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“…(Horgan 2004; Mao et al 2010; Wright and Ramesh 2012) Other studies did note a slight increase in axon tensile strains when gray and white matter property distinctions were included compared to global isotropy, (Cloots et al 2012; Cloots et al 2013; Colgan et al 2010) however, these differences were small when compared with differences between maximum principal tissue strain and tract-oriented strain. (Giordano et al 2014) Importantly, when we compare our oriented axonal strain injury thresholds to in vitro thresholds, we find very good concurrence, underscoring that the axon-oriented strain distribution is resolved reasonably well with the isotropic model.…”

Section: Limitationssupporting

confidence: 57%

White matter tract-oriented deformation predicts traumatic axonal brain injury and reveals rotational direction-specific vulnerabilities

Sullivan

Eucker

Gabrieli

et al. 2014

Biomech Model Mechanobiol

142

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A systematic correlation between finite element models (FEMs) and histopathology is needed to define deformation thresholds associated with traumatic brain injury (TBI). In this study, a FEM of a transected piglet brain was used to reverse engineer the range of optimal shear moduli for infant (5-day-old, 553-658 Pa) and 4-week old toddler piglet brain, (692-811 Pa) from comparisons with measured in situ tissue strains. The more mature brain modulus was found to have significant strain and strain rate dependencies not observed with the infant brain. Age-appropriate FEMs were then used to simulate experimental TBI in infant (n=36) and pre-adolescent (n=17) piglets undergoing a range of rotational head loads. The experimental animals were evaluated for the presence of clinically significant traumatic axonal injury (TAI), which was then correlated with FEM-calculated measures of overall and white matter tract-oriented tissue deformations, and used to identify the metric with the highest sensitivity and specificity for detecting TAI. The best predictors of TAI were the tract-oriented strain (6–7%), strain rate (38–40 s−1), and strain times strain rate (1.3–1.8 s−1) values exceeded by 90% of the brain. These tract-oriented strain and strain rate thresholds for TAI were comparable to those found in isolated axonal stretch studies. Furthermore, we proposed that the higher degree of agreement between tissue distortion aligned with white matter tracts and TAI may be the underlying mechanism responsible for more severe TAI after horizontal and sagittal head rotations in our porcine model of nonimpact TAI than coronal plane rotations.

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Section: Limitationssupporting

confidence: 57%

White matter tract-oriented deformation predicts traumatic axonal brain injury and reveals rotational direction-specific vulnerabilities

Sullivan

Eucker

Gabrieli

et al. 2014

Biomech Model Mechanobiol

142

View full text Add to dashboard Cite

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“…54 This is unlikely to significantly alter the relative magnitudes of the different WM injury susceptibility indices we established, however. On the other hand, it must be recognized that brain material properties represent only a narrow subset of the many variables important to predict injury (others include, e.g., injury tolerances, on-field impacts, neuroimaging, and clinical diagnosis of concussion, etc.).…”

mentioning

confidence: 93%

“…First, the fiber strain magnitude appears to be dominated by WM structural anisotropy rather than material anisotropy, 54 suggesting that focusing on the former via tractography is appropriate for our current ''technique development'' study. Second, although the baseline DHIM is subject-specific, we intend to use it for population-based studies as well-e.g., via the pre-computed brain response atlas (pcBRA 32,46,76 ).…”

mentioning

confidence: 99%

White Matter Injury Susceptibility via Fiber Strain Evaluation Using Whole-Brain Tractography

Zhao

Ford

Flashman

et al. 2016

Journal of Neurotrauma

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Microscale brain injury studies suggest axonal elongation as a potential mechanism for diffuse axonal injury (DAI). Recent studies have begun to incorporate white matter (WM) structural anisotropy in injury analysis, with initial evidence suggesting improved injury prediction performance. In this study, we further develop a tractography-based approach to analyze fiber strains along the entire lengths of fibers from voxel-or anatomically constrained whole-brain tractography. This technique potentially extends previous element-or voxel-based methods that instead utilize WM fiber orientations averaged from typically coarse elements or voxels. Perhaps more importantly, incorporating tractography-based axonal structural information enables assessment of the overall injury risks to functionally important neural pathways and the anatomical regions they connect, which is not possible with previous methods. A DAI susceptibility index was also established to quantify voxel-wise WM local structural integrity and tract-wise damage of individual neural pathways. This ''graded'' injury susceptibility potentially extends the commonly employed treatment of injury as a simple binary condition. As an illustration, we evaluate the DAI susceptibilities of WM voxels and transcallosal fiber tracts in three idealized head impacts. Findings suggest the potential importance of the tractography-based approach for injury prediction. These efforts may enable future studies to correlate WM mechanical responses with neuroimaging, cognitive alteration, and concussion, and to reveal the relative vulnerabilities of neural pathways and identify the most vulnerable ones in real-world head impacts.

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“…Details about model validation are reported in “Appendix 1.” Further detail can be found in the publication by Giordano et al. (2014), Giordano and Kleiven (2014), Giordano and Kleiven (2016). Tables 1, 2 and 3 describe the material models used in the simulations.…”

Section: Methodsmentioning

confidence: 99%

“…(2015) was that the anisotropic properties of the brain were extracted from diffusion data of a single healthy subject (Giordano et al. 2014) or from average diffusion data of 12 healthy subjects (Sahoo et al. 2015).…”

Section: Introductionmentioning

confidence: 99%

Anisotropic finite element models for brain injury prediction: the sensitivity of axonal strain to white matter tract inter-subject variability

Giordano

Zappalá

Kleiven

2017

Biomech Model Mechanobiol

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Computational models incorporating anisotropic features of brain tissue have become a valuable tool for studying the occurrence of traumatic brain injury. The tissue deformation in the direction of white matter tracts (axonal strain) was repeatedly shown to be an appropriate mechanical parameter to predict injury. However, when assessing the reliability of axonal strain to predict injury in a population, it is important to consider the predictor sensitivity to the biological inter-subject variability of the human brain. The present study investigated the axonal strain response of 485 white matter subject-specific anisotropic finite element models of the head subjected to the same loading conditions. It was observed that the biological variability affected the orientation of the preferential directions (coefficient of variation of 39.41% for the elevation angle—coefficient of variation of 29.31% for the azimuth angle) and the determination of the mechanical fiber alignment parameter in the model (gray matter volume 55.55–70.75%). The magnitude of the maximum axonal strain showed coefficients of variation of 11.91%. On the contrary, the localization of the maximum axonal strain was consistent: the peak of strain was typically located in a 2 cm3 volume of the brain. For a sport concussive event, the predictor was capable of discerning between non-injurious and concussed populations in several areas of the brain. It was concluded that, despite its sensitivity to biological variability, axonal strain is an appropriate mechanical parameter to predict traumatic brain injury.

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The influence of anisotropy on brain injury prediction

Cited by 93 publications

References 20 publications

White matter tract-oriented deformation predicts traumatic axonal brain injury and reveals rotational direction-specific vulnerabilities

White matter tract-oriented deformation predicts traumatic axonal brain injury and reveals rotational direction-specific vulnerabilities

White Matter Injury Susceptibility via Fiber Strain Evaluation Using Whole-Brain Tractography

Anisotropic finite element models for brain injury prediction: the sensitivity of axonal strain to white matter tract inter-subject variability

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