Anisotropic mechanical properties in the healthy human brain estimated with multi-excitation transversely isotropic MR elastography

Smith, Daniel R.; Caban-Rivera, Diego A.; McGarry, Matthew; Williams, L. Tyler; McIlvain, Grace; Okamoto, Ruth J.; Houten, Elijah E. W. Van; Bayly, Philip V.; Paulsen, Keith D.; Johnson, Curtis L.

doi:10.1016/j.brain.2022.100051

Cited by 18 publications

(16 citation statements)

References 57 publications

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“…In this study, measurements of shear stiffness and shear anisotropy were relatively similar to results from previous reports in the MRE literature with similar vibration frequencies (m 1 = 1.26 -1.32 kPa , m 2 = 1.53 -2.00 kPa, and f = 0.18 -0.59) (Green et al 2013, Guo et al 2016, Babaei et al 2021). The repeatability of the estimated shear moduli were for the repeated measurements of a single subject averaging 5.0% in experiment 1 and 10.9% in experiment 2 (Johnson et al 2013, Smith et al 2022. None of the prior published studies reported z as a material parameter; hence, comparisons were not possible with the data presented here.…”

Section: Discussionmentioning

confidence: 68%

In vivo estimation of anisotropic mechanical properties of the gastrocnemius during functional loading with MR elastography

Smith¹,

Caban-Rivera²,

Williams³

et al. 2023

Phys. Med. Biol.

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Objective: In-vivo imaging assessments of skeletal muscle structure and function allow for longitudinal quantification of tissue health. Magnetic resonance elastography (MRE) non-invasively quantifies tissue mechanical properties, allowing for evaluation of skeletal muscle biomechanics in response to loading, creating a better understanding of muscle functional health. Approach: In this study, we analyze the anisotropic mechanical response of calf muscles using MRE with a transversely isotropic, nonlinear inversion algorithm (TI-NLI) to investigate the role of muscle fiber stiffening under load. We estimate anisotropic material parameters including fiber shear stiffness (μ1), substrate shear stiffness (μ2), shear anisotropy (ϕ), and tensile anisotropy (ζ) of the gastrocnemius muscle in response to both passive and active tension. Main Results: In passive tension, we found a significant increase in μ1, ϕ, and ζ with increasing muscle length. While in active tension, we observed increasing μ2 and decreasing ϕ and ζ during active dorsiflexion and plantarflexion – indicating less anisotropy – with greater effects when the muscles act as agonist. Significance: The study demonstrates the ability of this anisotropic MRE method to capture the multifaceted mechanical response of skeletal muscle to tissue loading from muscle lengthening and contraction.

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Section: Discussionmentioning

confidence: 68%

In vivo estimation of anisotropic mechanical properties of the gastrocnemius during functional loading with MR elastography

Smith¹,

Caban-Rivera²,

Williams³

et al. 2023

Phys. Med. Biol.

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“…In the adult brain, higher global shear stiffness corresponds to healthier tissue, and stiffness decreases with age (reviewed in Hiscox et al., 2021) and in neurodegenerative conditions including multiple sclerosis (Streitberger et al., 2012; Wuerfel et al., 2010) and Alzheimer's disease (Hiscox et al., 2020; Murphy et al., 2011). White matter is stiffer than gray matter in healthy adults (Johnson, McGarry, Van Houten, et al., 2013; van Dommelen et al., 2010), and within white matter, highly organized tracts such as corpus callosum are stiffest (Smith, Caban‐Rivera, et al., 2022). Damping ratio, a dimensionless parameter that describes motion attenuation due to energy dissipation, is lower in highly organized white matter tracts such as corpus callosum (Johnson, McGarry, Gharibans, et al., 2013).…”

Section: Introductionmentioning

confidence: 99%

“…White matter is stiffer than gray matter in healthy adults (Johnson, McGarry, Van Houten, et al, 2013;van Dommelen et al, 2010), and within white matter, highly organized tracts such as corpus callosum are stiffest (Smith, Caban-Rivera, et al, 2022). Damping ratio, a dimensionless parameter that describes motion attenuation due to energy dissipation, is lower in highly organized white matter tracts such as corpus callosum (Johnson, McGarry, Gharibans, et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Magnetic resonance elastography captures a transient benefit of exercise intervention on forebrain stiffness in a rat model of fetal alcohol spectrum disorders

Milbocker,

Williams,

Caban‐Rivera

et al. 2024

Alcohol, Clinical and Experimental Research

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BackgroundFetal alcohol spectrum disorders (FASD), a group of prevalent conditions resulting from prenatal alcohol exposure, affect the maturation of cerebral white matter as first identified with neuroimaging. However, traditional methods are unable to track subtle microstructural alterations to white matter. This preliminary study uses a highly sensitive and clinically translatable magnetic resonance elastography (MRE) protocol to assess brain tissue microstructure through its mechanical properties following an exercise intervention in a rat model of FASD.MethodsFemale rat pups were either alcohol‐exposed (AE) via intragastric intubation of alcohol in milk substitute (5.25 g/kg/day) or sham‐intubated (SI) on postnatal days (PD) four through nine to model alcohol exposure during the brain growth spurt. On PD 30, half of AE and SI rats were randomly assigned to either a wheel‐running or standard cage for 12 days. Magnetic resonance elastography was used to measure whole brain and callosal mechanical properties at the end of the intervention (around PD 42) and at 1 month post‐intervention, and findings were validated with histological quantification of oligoglia.ResultsAlcohol exposure reduced forebrain stiffness (p = 0.02) in standard‐housed rats. The adolescent exercise intervention mitigated this effect, confirming that increased aerobic activity supports proper neurodevelopmental trajectories. Forebrain damping ratio was lowest in standard‐housed AE rats (p < 0.01), but this effect was not mitigated by intervention exposure. At 1 month post‐intervention, all rats exhibited comparable forebrain stiffness and damping ratio (p > 0.05). Callosal stiffness and damping ratio increased with age. With cessation of exercise, there was a negative rebound effect on the quantity of callosal oligodendrocytes, irrespective of treatment group, which diverged from our MRE results.ConclusionsThis is the first application of MRE to measure the brain's mechanical properties in a rodent model of FASD. MRE successfully captured alcohol‐related changes in forebrain stiffness and damping ratio. Additionally, MRE identified an exercise‐related increase to forebrain stiffness in AE rats.

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“…Shear waves in fibrous, transversely-isotropic materials travel at different wave speeds based on wave propagation and polarization directions (Tweten et al, 2015), and, as such, MRE displacement data must deform the tissue of interest in multiple directions in order to estimate anisotropic parameters reliably (Tweten et al, 2017). Multi-excitation MRE uses two or more vibration sources, applied sequentially, to generate different wave patterns throughout the brain (Smith et al, 2020), and, when coupled with TI-NLI, produces repeatable anisotropic property estimates in WM tracts (Smith et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Mechanical Properties of White Matter Tracts in Aging Assessed via Anisotropic MR Elastography

Caban-Rivera,

Williams,

McGarry

et al. 2024

Preprint

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Magnetic resonance elastography (MRE) is a promising neuroimaging technique to probe tissue microstructure, which has revealed widespread softening with loss of structural integrity in the aging brain. Traditional MRE approaches assume mechanical isotropy. However, white matter is known to be anisotropic from aligned, myelinated axonal bundles, which can lead to uncertainty in mechanical property estimates in these areas when using isotropic MRE. Recent advances in anisotropic MRE now allow for estimation of shear and tensile anisotropy, along with substrate shear modulus, in white matter tracts. The objective of this study was to investigate age-related differences in anisotropic mechanical properties in human brain white matter tracts for the first time. Anisotropic mechanical properties in all tracts were found to be significantly lower in older adults compared to young adults, with average property differences ranging between 0.028-0.107 for shear anisotropy and between 0.139-0.347 for tensile anisotropy. Stiffness perpendicular to the axonal fiber direction was also significantly lower in older age, but only in certain tracts. When compared with fractional anisotropy measures from diffusion tensor imaging, we found that anisotropic MRE measures provided additional, complementary information in describing differences between the white matter integrity of young and older populations. Anisotropic MRE provides a new tool for studying white matter structural integrity in aging and neurodegeneration.

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Anisotropic mechanical properties in the healthy human brain estimated with multi-excitation transversely isotropic MR elastography

Cited by 18 publications

References 57 publications

In vivo estimation of anisotropic mechanical properties of the gastrocnemius during functional loading with MR elastography

In vivo estimation of anisotropic mechanical properties of the gastrocnemius during functional loading with MR elastography

Magnetic resonance elastography captures a transient benefit of exercise intervention on forebrain stiffness in a rat model of fetal alcohol spectrum disorders

Mechanical Properties of White Matter Tracts in Aging Assessed via Anisotropic MR Elastography

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