Abstract
Objectives
To analyze the mechanical properties in different regions of the brain in healthy adults in a wide age range: 26 to 76 years old.
Methods
We used a multifrequency magnetic resonance elastography (MRE) protocol to analyze the effect of age on frequency-dependent (storage and loss moduli, G′ and G″, respectively) and frequency-independent parameters (μ1, μ2, and η, as determined by a standard linear solid model) of the cerebral parenchyma, cortical gray matter (GM), white matter (WM), and subcortical GM structures of 46 healthy male and female subjects. The multifrequency behavior of the brain and frequency-independent parameters were analyzed across different age groups.
Results
The annual change rate ranged from − 0.32 to − 0.36% for G′ and − 0.43 to − 0.55% for G″ for the cerebral parenchyma, cortical GM, and WM. For the subcortical GM, changes in G′ ranged from − 0.18 to − 0.23%, and G″ changed − 0.43%. Interestingly, males exhibited decreased elasticity, while females exhibited decreased viscosity with respect to age in some regions of subcortical GM. Significantly decreased values were also found in subjects over 60 years old.
Conclusion
Values of G′ and G″ at 60 Hz and the frequency-independent μ2 of the caudate, putamen, and thalamus may serve as parameters that characterize the aging effect on the brain. The decrease in brain stiffness accelerates in elderly subjects.
Key Points
• We used a multifrequency MRE protocol to assess changes in the mechanical properties of the brain with age.
• Frequency-dependent (storage moduli G′ and loss moduli G″) and frequency-independent (μ1, μ2, and η) parameters can bequantitatively measured by our protocol.
• The decreased value of viscoelastic properties due to aging varies in different regions of subcortical GM in males and females, and the decrease in brain stiffness is accelerated in elderly subjects over 60 years old.
Similar content being viewed by others
Abbreviations
- AAL:
-
Automated anatomical labeling
- ANOVA :
-
Analysis of variance
- CSF:
-
Cerebrospinal fluid
- CT:
-
Computed tomography
- G′:
-
Storage moduli
- G″:
-
Loss moduli
- GE:
-
General Electric
- GM:
-
Gray matter
- LSD:
-
Least significant difference
- MEG:
-
Motion encoding gradient
- MNI:
-
Montreal Neurological Institute
- MRE:
-
Magnetic resonance elastography
- MRI:
-
Magnetic resonance imaging
- ROI :
-
Region of interest
- SD:
-
Standard deviation
- SEM:
-
Standard error of the mean
- WM:
-
White matter
References
Ophir J, Alam SK, Garra B et al (1999) Elastography: ultrasonic estimation and imaging of the elastic properties of tissues. Proc Inst Mech Eng H 213:203–233
Muthupillai R, Lomas DJ, Rossman PJ, Greenleaf JF, Manduca A, Ehman RL (1995) Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. Science 269:1854–1857
Muthupillai R, Ehman RL (1996) Magnetic resonance elastography. Nat Med 2:601–603
Hiscox LV, Johnson CL, Barnhill E et al (2016) Magnetic resonance elastography (MRE) of the human brain: technique, findings and clinical applications. Phys Med Biol 61:R401–R437
Glaser KJ, Manduca A, Ehman RL (2012) Review of MR elastography applications and recent developments. J Magn Reson Imaging 36:757–774
Di Ieva A, Grizzi F, Rognone E et al (2010) Magnetic resonance elastography: a general overview of its current and future applications in brain imaging. Neurosurg Rev 33:137–145
Murphy MC, Huston J 3rd, Ehman RL (2019) MR elastography of the brain and its application in neurological diseases. Neuroimage 187:176–183
Yin Z, Romano AJ, Manduca A, Ehman RL, Huston JR 3rd (2018) Stiffness and beyond: what MR elastography can tell us about brain structure and function under physiologic and pathologic conditions. Top Magn Reson Imaging 27:305–318
Arani A, Murphy MC, Glaser KJ et al (2015) Measuring the effects of aging and sex on regional brain stiffness with MR elastography in healthy older adults. Neuroimage 111:59–64
Sack I, Jöhrens K, Würfel J, Braun J (2013) Structure-sensitive elastography: on the viscoelastic powerlaw behavior of in vivo human tissue in health and disease. Soft Matter 9:5672–5680
Takamura T, Motosugi U, Sasaki Y et al (2020) Influence of age on global and regional brain stiffness in young and middle-aged adults. J Magn Reson Imaging 51:727–733
McIlvain G, Schwarb H, Cohen NJ, Telzer EH, Johnson CL (2018) Mechanical properties of the in vivo adolescent human brain. Dev Cogn Neurosci 34:27–33
Hiscox LV, Johnson CL, McGarry MDJ et al (2018) High-resolution magnetic resonance elastography reveals differences in subcortical gray matter viscoelasticity between young and healthy older adults. Neurobiol Aging 65:158–167
Johnson CL, Schwarb H, McGarry MDJ et al (2016) Viscoelasticity of subcortical gray matter structures. Hum Brain Mapp 37:4221–4233
Sack I, Beierbach B, Wuerfel J et al (2009) The impact of aging and gender on brain viscoelasticity. Neuroimage 46:652–657
Bunevicius A, Schregel K, Sinkus R, Golby A, Patz S (2019) Review: MR elastography of brain tumors. Neuroimage Clin 25:102109
Dittmann F, Hirsch S, Tzschätzsch H, Guo J, Braun J, Sack I (2016) In vivo wideband multifrequency MR elastography of the human brain and liver. Magn Reson Med 76:1116–1126
Feng Y, Clayton EH, Chang Y, Okamoto RJ, Bayly PV (2013) Viscoelastic properties of the ferret brain measured in vivo at multiple frequencies by magnetic resonance elastography. J Biomech 46:863–870
Klatt D, Hamhaber U, Asbach P, Braun J, Sack I (2007) Noninvasive assessment of the rheological behavior of human organs using multifrequency MR elastography: a study of brain and liver viscoelasticity. Phys Med Biol 52:7281–7294
Kurt M, Wu L, Laksari K et al (2019) Optimization of a multifrequency magnetic resonance elastography protocol for the human brain. J Neuroimaging 29:440–446
Sack I, Streitberger KJ, Krefting D, Paul F, Braun J (2011) The influence of physiological aging and atrophy on brain viscoelastic properties in humans. PLoS One 6:e23451
Squarzoni P, Duran FLS, Busatto GF, Alves TCTF (2018) Reduced gray matter volume of the thalamus and hippocampal region in elderly healthy adults with no impact of APOE varepsilon4: a longitudinal voxel-based morphometry study. J Alzheimers Dis 62:757–771
Raz N, Lindenberger U, Rodrigue KM et al (2005) Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 15:1676–1689
Weickenmeier J, Kurt M, Ozkaya E, Wintermark M, Pauly KB, Kuhl E (2018) Magnetic resonance elastography of the brain: a comparison between pigs and humans. J Mech Behav Biomed Mater 77:702–710
Mehmet K, Han L, Kaveh L et al (2016) In vivo multi-frequency magnetic resonance elastography of the human brain: which frequencies matter? Biomedical Engineering Society Annual Meeting, Phoenix
Chartrain AG, Kurt M, Yao A et al (2019) Utility of preoperative meningioma consistency measurement with magnetic resonance elastography (MRE): a review. Neurosurg Rev 42:1–7
Murphy MC, Huston JR, Jack CR Jr et al (2011) Decreased brain stiffness in Alzheimer's disease determined by magnetic resonance elastography. J Magn Reson Imaging 34:494–498
Tzouriomazoyer N, Landeau B, Papathanassiou D et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273
Oliphant TE, Manduca A, Ehman RL, Greenleaf JF (2001) Complex-valued stiffness reconstruction for magnetic resonance elastography by algebraic inversion of the differential equation. Magn Reson Med 45:299–310
Fung YC, Cowin SC (1994) Biomechanics: mechanical properties of living tissues, 2nd edn. Springer Science+Business Media, Berlin
Munder T, Pfeffer A, Schreyer S et al (2018) MR elastography detection of early viscoelastic response of the murine hippocampus to amyloid beta accumulation and neuronal cell loss due to Alzheimer’s disease. J Magn Reson Imaging 47:105–114
Murphy MC, Jones DT, Jack CR Jr et al (2016) Regional brain stiffness changes across the Alzheimer’s disease spectrum. Neuroimage Clin 10:283–290
ElSheikh M, Arani A, Perry A et al (2017) MR elastography demonstrates unique regional brain stiffness patterns in dementias. AJR Am J Roentgenol 209:403–408
Streitberger KJ, Fehlner A, Pache F et al (2017) Multifrequency magnetic resonance elastography of the brain reveals tissue degeneration in neuromyelitis optica spectrum disorder. Eur Radiol 27:2206–2215
Huston JR 3rd, Murphy MC, Boeve BF et al (2016) Magnetic resonance elastography of frontotemporal dementia. J Magn Reson Imaging 43:474–478
Riek K, Millward JM, Hamann I et al (2012) Magnetic resonance elastography reveals altered brain viscoelasticity in experimental autoimmune encephalomyelitis. Neuroimage Clin 1:81–90
Weickenmeier J, Kurt M, Ozkaya E et al (2018) Brain stiffens post mortem. J Mech Behav Biomed Mater 84:88–98
Guo J, Bertalan G, Meierhofer D et al (2019) Brain maturation is associated with increasing tissue stiffness and decreasing tissue fluidity. Acta Biomater 99:433–442
Javid A, Wei Z, Carissa G et al (2019) Nonlinear dynamical behavior of the deep white matter during head impact. Phys Rev Appl. https://doi.org/10.1103/PhysRevApplied.12.014058
Laksari K, Kurt M, Babaee H, Kleiven S, Camarillo DR (2018) Mechanistic insights into human brain impact dynamics through modal analysis. Phys Rev Lett 120:138101
Johnson CL, Telzer EH (2018) Magnetic resonance elastography for examining developmental changes in the mechanical properties of the brain. Dev Cogn Neurosci 33:176–181
Acknowledgments
We thank Richard L. Ehman from the Mayo Clinic Rochester for providing the MRE activation device. We acknowledge Karla Epperson, Kevin Epperson, and Anne M. Sawyer from the Richard M. Lucas Center, Stanford University for their support during the experiments.
Funding
This work was supported by Grant No. 61801311 from the National Natural Science Foundation of China, Grant No. 7182044 from Beijing Natural Science Foundation, No. PX2018001 from Beijing Hospitals Authority, QML20180103 from Beijing Hospitals Authority Youth Programme, No. YYZZ2017B01 from Beijing Friendship Hospital, Capital Medical University, and No. 2019 M660717 from China Postdoctoral Science Foundation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Guarantor
The scientific guarantor of this publication is Max Wintermark.
Conflict of interest
The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.
Statistics and biometry
One of the authors has significant statistical expertise.
Informed consent
Written informed consent was obtained from all subjects (patients) in this study.
Ethical approval
Institutional Review Board approval was obtained.
Methodology
• retrospective
• cross-sectional study
• performed at one institution
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 133 kb)
Rights and permissions
About this article
Cite this article
Lv, H., Kurt, M., Zeng, N. et al. MR elastography frequency–dependent and independent parameters demonstrate accelerated decrease of brain stiffness in elder subjects. Eur Radiol 30, 6614–6623 (2020). https://doi.org/10.1007/s00330-020-07054-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-020-07054-7