Decreased tissue stiffness in glioblastoma by MR elastography is associated with increased cerebral blood flow

Siri Fløgstad Svensson; Elies Fuster-Garcia; Anna Latysheva; Jorunn Fraser-Green; Wibeke Nordhøy; Omar Isam Darwish; Ivar Thokle Hovden; Sverre Holm; Einar O. Vik-Mo; Ralph Sinkus; Kyrre Eeg Emblem

doi:10.1016/j.ejrad.2021.110136

Decreased tissue stiffness in glioblastoma by MR elastography is associated with increased cerebral blood flow

Siri Fløgstad Svensson^*, Elies Fuster-Garcia, Anna Latysheva, Jorunn Fraser-Green, Wibeke Nordhøy, Omar Isam Darwish, Ivar Thokle Hovden, Sverre Holm, Einar O. Vik-Mo, Ralph Sinkus, Kyrre Eeg Emblem

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

23 Citations (Scopus)

Abstract

Purpose: Understanding how mechanical properties relate to functional changes in glioblastomas may help explain different treatment response between patients. The aim of this study was to map differences in biomechanical and functional properties between tumor and healthy tissue, to assess any relationship between them and to study their spatial distribution. Methods: Ten patients with glioblastoma and 17 healthy subjects were scanned using MR Elastography, perfusion and diffusion MRI. Stiffness and viscosity measurements G′ and G′′, cerebral blood flow (CBF), apparent diffusion coefficient (ADC) and fractional anisotropy (FA) were measured in patients’ contrast-enhancing tumor, necrosis, edema, and gray and white matter, and in gray and white matter for healthy subjects. A regression analysis was used to predict CBF as a function of ADC, FA, G′ and G′′. Results: Median G′ and G′′ in contrast-enhancing tumor were 13% and 37% lower than in normal-appearing white matter (P < 0.01), and 8% and 6% lower in necrosis than in contrast-enhancing tumor, respectively (P < 0.05). Tumors showed both inter-patient and intra-patient heterogeneity. Measurements approached values in normal-appearing tissue when moving outward from the tumor core, but abnormal tissue properties were still present in regions of normal-appearing tissue. Using both a linear and a random-forest model, prediction of CBF was improved by adding MRE measurements to the model (P < 0.01). Conclusions: The inclusion of MRE measurements in statistical models helped predict perfusion, with stiffer tissue associated with lower perfusion values.

Original language	English
Article number	110136
Journal	European Journal of Radiology
Volume	147
DOIs	https://doi.org/10.1016/j.ejrad.2021.110136
Publication status	Published - Feb 2022

Keywords

Brain tumor
Glioblastoma
Magnetic Resonance Elastography
Tumor stiffness
Viscoelastic properties

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10.1016/j.ejrad.2021.110136

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Fløgstad Svensson, S., Fuster-Garcia, E., Latysheva, A., Fraser-Green, J., Nordhøy, W., Isam Darwish, O., Thokle Hovden, I., Holm, S., Vik-Mo, E. O., Sinkus, R., & Eeg Emblem, K. (2022). Decreased tissue stiffness in glioblastoma by MR elastography is associated with increased cerebral blood flow. European Journal of Radiology, 147, Article 110136. https://doi.org/10.1016/j.ejrad.2021.110136

@article{bc7b0efbebcf4639b2c8069bd7564391,

title = "Decreased tissue stiffness in glioblastoma by MR elastography is associated with increased cerebral blood flow",

abstract = "Purpose: Understanding how mechanical properties relate to functional changes in glioblastomas may help explain different treatment response between patients. The aim of this study was to map differences in biomechanical and functional properties between tumor and healthy tissue, to assess any relationship between them and to study their spatial distribution. Methods: Ten patients with glioblastoma and 17 healthy subjects were scanned using MR Elastography, perfusion and diffusion MRI. Stiffness and viscosity measurements G′ and G′′, cerebral blood flow (CBF), apparent diffusion coefficient (ADC) and fractional anisotropy (FA) were measured in patients{\textquoteright} contrast-enhancing tumor, necrosis, edema, and gray and white matter, and in gray and white matter for healthy subjects. A regression analysis was used to predict CBF as a function of ADC, FA, G′ and G′′. Results: Median G′ and G′′ in contrast-enhancing tumor were 13% and 37% lower than in normal-appearing white matter (P < 0.01), and 8% and 6% lower in necrosis than in contrast-enhancing tumor, respectively (P < 0.05). Tumors showed both inter-patient and intra-patient heterogeneity. Measurements approached values in normal-appearing tissue when moving outward from the tumor core, but abnormal tissue properties were still present in regions of normal-appearing tissue. Using both a linear and a random-forest model, prediction of CBF was improved by adding MRE measurements to the model (P < 0.01). Conclusions: The inclusion of MRE measurements in statistical models helped predict perfusion, with stiffer tissue associated with lower perfusion values.",

keywords = "Brain tumor, Glioblastoma, Magnetic Resonance Elastography, Tumor stiffness, Viscoelastic properties",

author = "{Fl{\o}gstad Svensson}, Siri and Elies Fuster-Garcia and Anna Latysheva and Jorunn Fraser-Green and Wibeke Nordh{\o}y and {Isam Darwish}, Omar and {Thokle Hovden}, Ivar and Sverre Holm and Vik-Mo, {Einar O.} and Ralph Sinkus and {Eeg Emblem}, Kyrre",

note = "Funding Information: Grant Support: We gratefully acknowledge support from the European Union{\textquoteright}s Horizon 2020 Programme: ERC Grant Agreement No. 758657-ImPRESS, Research and Innovation Grant Agreements No. 668039-FORCE and Marie Sk{\l}odowska-Curie grant agreement (No 844646-GLIOHAB), South-Eastern Norway Regional Health Authority (Grant Agreement No. 2017073, 2013069 and 2021057), The Research Council of Norway FRIPRO (Grant Agreement No. 261984), the National Institutes of Health R21 grant (Grant Agreement No. EB030757), and the German Research Foundation (DFG, SCHR 1542/1-1). Funding Information: Grant Support: We gratefully acknowledge support from the European Union's Horizon 2020 Programme: ERC Grant Agreement No. 758657-ImPRESS, Research and Innovation Grant Agreements No. 668039-FORCE and Marie Sk{\l}odowska-Curie grant agreement (No 844646-GLIOHAB), South-Eastern Norway Regional Health Authority (Grant Agreement No. 2017073, 2013069 and 2021057), The Research Council of Norway FRIPRO (Grant Agreement No. 261984), the National Institutes of Health R21 grant (Grant Agreement No. EB030757), and the German Research Foundation (DFG, SCHR 1542/1-1). Publisher Copyright: {\textcopyright} 2022 The Authors",

year = "2022",

month = feb,

doi = "10.1016/j.ejrad.2021.110136",

language = "English",

volume = "147",

journal = "European Journal of Radiology",

issn = "0720-048X",

publisher = "Elsevier",

}

Fløgstad Svensson, S, Fuster-Garcia, E, Latysheva, A, Fraser-Green, J, Nordhøy, W, Isam Darwish, O, Thokle Hovden, I, Holm, S, Vik-Mo, EO, Sinkus, R & Eeg Emblem, K 2022, 'Decreased tissue stiffness in glioblastoma by MR elastography is associated with increased cerebral blood flow', European Journal of Radiology, vol. 147, 110136. https://doi.org/10.1016/j.ejrad.2021.110136

TY - JOUR

T1 - Decreased tissue stiffness in glioblastoma by MR elastography is associated with increased cerebral blood flow

AU - Fløgstad Svensson, Siri

AU - Fuster-Garcia, Elies

AU - Latysheva, Anna

AU - Fraser-Green, Jorunn

AU - Nordhøy, Wibeke

AU - Isam Darwish, Omar

AU - Thokle Hovden, Ivar

AU - Holm, Sverre

AU - Vik-Mo, Einar O.

AU - Sinkus, Ralph

AU - Eeg Emblem, Kyrre

N1 - Funding Information: Grant Support: We gratefully acknowledge support from the European Union’s Horizon 2020 Programme: ERC Grant Agreement No. 758657-ImPRESS, Research and Innovation Grant Agreements No. 668039-FORCE and Marie Skłodowska-Curie grant agreement (No 844646-GLIOHAB), South-Eastern Norway Regional Health Authority (Grant Agreement No. 2017073, 2013069 and 2021057), The Research Council of Norway FRIPRO (Grant Agreement No. 261984), the National Institutes of Health R21 grant (Grant Agreement No. EB030757), and the German Research Foundation (DFG, SCHR 1542/1-1). Funding Information: Grant Support: We gratefully acknowledge support from the European Union's Horizon 2020 Programme: ERC Grant Agreement No. 758657-ImPRESS, Research and Innovation Grant Agreements No. 668039-FORCE and Marie Skłodowska-Curie grant agreement (No 844646-GLIOHAB), South-Eastern Norway Regional Health Authority (Grant Agreement No. 2017073, 2013069 and 2021057), The Research Council of Norway FRIPRO (Grant Agreement No. 261984), the National Institutes of Health R21 grant (Grant Agreement No. EB030757), and the German Research Foundation (DFG, SCHR 1542/1-1). Publisher Copyright: © 2022 The Authors

PY - 2022/2

Y1 - 2022/2

N2 - Purpose: Understanding how mechanical properties relate to functional changes in glioblastomas may help explain different treatment response between patients. The aim of this study was to map differences in biomechanical and functional properties between tumor and healthy tissue, to assess any relationship between them and to study their spatial distribution. Methods: Ten patients with glioblastoma and 17 healthy subjects were scanned using MR Elastography, perfusion and diffusion MRI. Stiffness and viscosity measurements G′ and G′′, cerebral blood flow (CBF), apparent diffusion coefficient (ADC) and fractional anisotropy (FA) were measured in patients’ contrast-enhancing tumor, necrosis, edema, and gray and white matter, and in gray and white matter for healthy subjects. A regression analysis was used to predict CBF as a function of ADC, FA, G′ and G′′. Results: Median G′ and G′′ in contrast-enhancing tumor were 13% and 37% lower than in normal-appearing white matter (P < 0.01), and 8% and 6% lower in necrosis than in contrast-enhancing tumor, respectively (P < 0.05). Tumors showed both inter-patient and intra-patient heterogeneity. Measurements approached values in normal-appearing tissue when moving outward from the tumor core, but abnormal tissue properties were still present in regions of normal-appearing tissue. Using both a linear and a random-forest model, prediction of CBF was improved by adding MRE measurements to the model (P < 0.01). Conclusions: The inclusion of MRE measurements in statistical models helped predict perfusion, with stiffer tissue associated with lower perfusion values.

AB - Purpose: Understanding how mechanical properties relate to functional changes in glioblastomas may help explain different treatment response between patients. The aim of this study was to map differences in biomechanical and functional properties between tumor and healthy tissue, to assess any relationship between them and to study their spatial distribution. Methods: Ten patients with glioblastoma and 17 healthy subjects were scanned using MR Elastography, perfusion and diffusion MRI. Stiffness and viscosity measurements G′ and G′′, cerebral blood flow (CBF), apparent diffusion coefficient (ADC) and fractional anisotropy (FA) were measured in patients’ contrast-enhancing tumor, necrosis, edema, and gray and white matter, and in gray and white matter for healthy subjects. A regression analysis was used to predict CBF as a function of ADC, FA, G′ and G′′. Results: Median G′ and G′′ in contrast-enhancing tumor were 13% and 37% lower than in normal-appearing white matter (P < 0.01), and 8% and 6% lower in necrosis than in contrast-enhancing tumor, respectively (P < 0.05). Tumors showed both inter-patient and intra-patient heterogeneity. Measurements approached values in normal-appearing tissue when moving outward from the tumor core, but abnormal tissue properties were still present in regions of normal-appearing tissue. Using both a linear and a random-forest model, prediction of CBF was improved by adding MRE measurements to the model (P < 0.01). Conclusions: The inclusion of MRE measurements in statistical models helped predict perfusion, with stiffer tissue associated with lower perfusion values.

KW - Brain tumor

KW - Glioblastoma

KW - Magnetic Resonance Elastography

KW - Tumor stiffness

KW - Viscoelastic properties

UR - http://www.scopus.com/inward/record.url?scp=85122507961&partnerID=8YFLogxK

U2 - 10.1016/j.ejrad.2021.110136

DO - 10.1016/j.ejrad.2021.110136

M3 - Article

AN - SCOPUS:85122507961

SN - 0720-048X

VL - 147

JO - European Journal of Radiology

JF - European Journal of Radiology

M1 - 110136

ER -

Decreased tissue stiffness in glioblastoma by MR elastography is associated with increased cerebral blood flow

Abstract

Keywords

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