Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
European Radiology
Published in: European Radiology 12/2020

01-12-2020 | Magnetic Resonance

MR elastography frequency–dependent and independent parameters demonstrate accelerated decrease of brain stiffness in elder subjects

Authors: Han Lv, Mehmet Kurt, Na Zeng, Efe Ozkaya, Fabiola Marcuz, Lyndia Wu, Kaveh Laksari, David B. Camarillo, Kim Butts Pauly, Zhenchang Wang, Max Wintermark

Published in: European Radiology | Issue 12/2020

Login to get access

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.
Appendix
Available only for authorised users
Literature
1.
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 213:203–233CrossRef
2.
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
3.
Muthupillai R, Ehman RL (1996) Magnetic resonance elastography. Nat Med 2:601–603CrossRef
4.
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–R437CrossRef
5.
Glaser KJ, Manduca A, Ehman RL (2012) Review of MR elastography applications and recent developments. J Magn Reson Imaging 36:757–774CrossRef
6.
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 33:137–145CrossRef
7.
Murphy MC, Huston J 3rd, Ehman RL (2019) MR elastography of the brain and its application in neurological diseases. Neuroimage 187:176–183
8.
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
9.
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 111:59–64CrossRef
10.
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
11.
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 51:727–733CrossRef
12.
McIlvain G, Schwarb H, Cohen NJ, Telzer EH, Johnson CL (2018) Mechanical properties of the in vivo adolescent human brain. Dev Cogn Neurosci 34:27–33CrossRef
13.
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 65:158–167CrossRef
14.
Johnson CL, Schwarb H, McGarry MDJ et al (2016) Viscoelasticity of subcortical gray matter structures. Hum Brain Mapp 37:4221–4233CrossRef
15.
Sack I, Beierbach B, Wuerfel J et al (2009) The impact of aging and gender on brain viscoelasticity. Neuroimage 46:652–657CrossRef
16.
Bunevicius A, Schregel K, Sinkus R, Golby A, Patz S (2019) Review: MR elastography of brain tumors. Neuroimage Clin 25:102109CrossRef
17.
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
18.
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 46:863–870CrossRef
19.
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 52:7281–7294CrossRef
20.
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
21.
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
22.
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 62:757–771CrossRef
23.
Raz N, Lindenberger U, Rodrigue KM et al (2005) Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 15:1676–1689CrossRef
24.
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
25.
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
26.
Chartrain AG, Kurt M, Yao A et al (2019) Utility of preoperative meningioma consistency measurement with magnetic resonance elastography (MRE): a review. Neurosurg Rev 42:1–7CrossRef
27.
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
28.
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 15:273CrossRef
29.
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 45:299–310CrossRef
30.
Fung YC, Cowin SC (1994) Biomechanics: mechanical properties of living tissues, 2nd edn. Springer Science+Business Media, Berlin
31.
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 47:105–114CrossRef
32.
Murphy MC, Jones DT, Jack CR Jr et al (2016) Regional brain stiffness changes across the Alzheimer’s disease spectrum. Neuroimage Clin 10:283–290CrossRef
33.
ElSheikh M, Arani A, Perry A et al (2017) MR elastography demonstrates unique regional brain stiffness patterns in dementias. AJR Am J Roentgenol 209:403–408CrossRef
34.
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 27:2206–2215CrossRef
35.
Huston JR 3rd, Murphy MC, Boeve BF et al (2016) Magnetic resonance elastography of frontotemporal dementia. J Magn Reson Imaging 43:474–478
36.
Riek K, Millward JM, Hamann I et al (2012) Magnetic resonance elastography reveals altered brain viscoelasticity in experimental autoimmune encephalomyelitis. Neuroimage Clin 1:81–90CrossRef
37.
Weickenmeier J, Kurt M, Ozkaya E et al (2018) Brain stiffens post mortem. J Mech Behav Biomed Mater 84:88–98CrossRef
38.
Guo J, Bertalan G, Meierhofer D et al (2019) Brain maturation is associated with increasing tissue stiffness and decreasing tissue fluidity. Acta Biomater 99:433–442CrossRef
39.
40.
Laksari K, Kurt M, Babaee H, Kleiven S, Camarillo DR (2018) Mechanistic insights into human brain impact dynamics through modal analysis. Phys Rev Lett 120:138101CrossRef
41.
Johnson CL, Telzer EH (2018) Magnetic resonance elastography for examining developmental changes in the mechanical properties of the brain. Dev Cogn Neurosci 33:176–181CrossRef
Metadata
Title
MR elastography frequency–dependent and independent parameters demonstrate accelerated decrease of brain stiffness in elder subjects
Authors
Han Lv
Mehmet Kurt
Na Zeng
Efe Ozkaya
Fabiola Marcuz
Lyndia Wu
Kaveh Laksari
David B. Camarillo
Kim Butts Pauly
Zhenchang Wang
Max Wintermark
Publication date
01-12-2020
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 12/2020
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-020-07054-7

Other articles of this Issue 12/2020

European Radiology 12/2020 Go to the issue

Forensic Medicine

Forensic age estimation in living adolescents with CT imaging of the clavicula—impact of low-dose scanning on readers’ confidence

Neuro

Vessel-selective 4D-MR angiography using super-selective pseudo-continuous arterial spin labeling may be a useful tool for assessing brain AVM hemodynamics

Correction

Correction to: A quantitative imaging biomarker for predicting disease-free-survival-associated histologic subgroups in lung adenocarcinoma

Chest

A predictive model and scoring system combining clinical and CT characteristics for the diagnosis of COVID-19

Interventional

Longitudinal study of interventional radiology activity in a large metropolitan Italian tertiary care hospital: how the COVID-19 pandemic emergency has changed our activity

Hepatobiliary-Pancreas

Comparison of a coaxial versus non-coaxial liver biopsy technique in an oncological setting: diagnostic yield, complications and seeding risk