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Skeletal muscle mechanical properties quantification: comparison between commercial ultrasound shear wave elastography and anisotropic magnetic resonance elastography
KTH, School of Engineering Sciences (SCI), Engineering Mechanics.ORCID iD: 0000-0003-2388-0365
Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden. Department of Medical Radiation Physics and Nuclear Medicine, Karolinska University Hospital, Stockholm, Sweden.
Department of Clinical and Experimental Sciences, University of Brescia, Italy.
Division of Paediatric Neurology, Department of Women’s and Children’s Health, Karolinska Institutet, Stockholm, Sweden. Department of Paediatric Orthopaedic Surgery and Paediatric Neurology, Astrid Lindgren Children’s Hospital, Karolinska University Hospital, Stockholm, Sweden.
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Background: Although elastography techniques, such as ultrasound shear wave elastography (SWE) and magnetic resonance elastography (MRE), are increasingly used to quantify mechanical properties of skeletal muscles, significant variation exists across the methods. These differences include measurement frequency ranges, post-processing approaches, and reported outcome parameters. This study aimed to compare the quantification of muscle mechanical properties between SWE and MRE.

Methods: SWE and MRE were performed on seven ex vivo muscle samples and medial gastrocnemius (MG) of nine able-bodied adults. Muscle anisotropic mechanical properties were quantified by estimating shear wave velocities (SWVs) parallel and perpendicular to the muscle fibers for ex vivo comparison. For in vivo comparison, only parallel SWV was assessed. Agreement between SWV estimation obtained from SWE and MRE was evaluated using Pearson correlation coefficient and the limit of agreement approach.

Results: SWV quantification using SWE and MRE demonstrated moderate to strong correlation in both ex vivo (perpendicular SWV: r = 0.777, p = 0.002, parallel SWV: r = 0.673, p = 0.012) and in vivo comparisons (parallel SWV: r = 0.707, p = 0.033). However, SWE consistently overestimated SWV compared to MRE across all conditions (average difference: perpendicular SWV ex vivo 0.42 m/s, parallel SWV ex vivo 0.67 m/s, parallel SWV in vivo: 0.53 m/s).

Conclusion: Muscle anisotropic mechanical property quantification using ultrasound SWE and MRE demonstrated good agreement in ex vivo muscle samples. In vivo, parallel SWV estimation from ultrasound SWE in pennate muscle showed good agreement with anisotropic MRE in able-bodied adult participants. 

Keywords [en]
Skeletal muscle, shear wave elastography, magnetic resonance elastography, animal
National Category
Radiology and Medical Imaging Medical Imaging
Identifiers
URN: urn:nbn:se:kth:diva-361813OAI: oai:DiVA.org:kth-361813DiVA, id: diva2:1948312
Note

QC 20250331

Available from: 2025-03-28 Created: 2025-03-28 Last updated: 2025-03-31Bibliographically approved
In thesis
1. Quantification of Skeletal Muscle Morphology and Mechanical Properties Using Medical Imaging
Open this publication in new window or tab >>Quantification of Skeletal Muscle Morphology and Mechanical Properties Using Medical Imaging
2025 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Skeletal muscle is crucial for enabling movement, maintaining posture, and stabilising joints. These functions are largely related to the morphology and mechanical properties of skeletal muscle. To quantify these properties in vivo, medical imaging techniques have been widely used, with ultrasonography and magnetic resonance imaging (MRI) being the most commonly used imaging modalities. This thesis presents four studies using different imaging techniques to quantify the morphology and mechanical properties of skeletal muscle. 

In the first study, we used three-dimensional freehand ultrasound (3DFUS) and MRI to quantify 3D skeletal muscle morphological parameters, including muscle volume, fascicle length, and pennation angle. We demonstrated that 3DFUS provided reliable and repeatable measurements, with strong agreement with MRI-based measurements. Given its lower cost and better accessibility, we suggest that 3DFUS could serve as a viable alternative to MRI for quantifying skeletal muscle morphology. 

In the second and third studies, we used two elastography techniques, magnetic resonance elastography (MRE) and ultrasound shear wave elastography (SWE), to quantify the mechanical properties of skeletal muscle. We incorporated diffusion tensor imaging to determine the fascicle orientation and integrated this information into the direct inversion of the wave equation in MRE. This approach allowed for the quantification of anisotropic mechanical properties under the assumption that skeletal muscle behaves as an incompressible transversely isotropic material. This approach was first validated through comparison with ex vivo rheometry measurements, demonstrating a good agreement between the two techniques, and then applied in vivo to the medial gastrocnemius (MG), demonstrating muscle anisotropy as well. We also compared this technique with a commercial ultrasound SWE system, which assumes skeletal muscle to be isotropic, by measuring both ex vivo muscle samples and the MG in vivo. By quantifying shear wave velocity using both elastography techniques, we observed a moderate to strong correlation between SWE and MRE in ex vivo muscle samples and a strong correlation in the MG in vivo. These findings suggested that the isotropy assumption in commercial ultrasound SWE systems does not substantially affect the quantification of muscle mechanical properties. 

In the fourth study, we used MRI to evaluate changes in calf muscle morphology and intramuscular fat content 12 months after the first botulinum neurotoxin type A (BoNT-A) injection in children with cerebral palsy (CP), who were naive to muscle tone reduction therapy. Our findings showed that the calf muscle growth was not impaired 12 months after BoNT-A injection, as indicated by increased absolute muscle volume and unchanged normalized muscle volume. However, the calf muscle growth was compromised by concurrent intramuscular fat infiltration, evidenced by increased intramuscular fat content. 

The ultrasonography and MRI techniques presented in this thesis provide the biomechanics field with different options for quantifying skeletal muscle morphology and mechanical properties. These techniques not only contribute to the medical imaging methodological development but also offer practical implications for clinical assessments and rehabilitation strategies.

Abstract [sv]

Skelettmuskulaturens funktion är viktigför förmågan att producera kraft som i kombination med neurologiska komponenter gör det möjligt för människan att röra sig, bibehålla hållningen och stabilisera lederna. Förmågan att producera kraft (ofta mätt som styrka) kan relateras till muskulaturensstruktur och mekaniska egenskaper. För att kvanitfiera dessa egenskaper in vivo används ofta medicinska avbildningstekniker varav ultraljud och magnetisk resonanstomografi (MRI) är de två mest använda metoderna. I denna avhandling som omfattar fyra studier presenteras olika avbildningstekniker för kvantifiering av skelettmuskulatur. 

I den första studien använde vi två tekniker, tredimensionell frihands-ultraljudsteknink (3DFUS) och MRI för 3D-kvantifiering av muskulaturens morfologiska egenskaper som inkluderade muskelvolym, fascikellängd och pennationsvinkel. Vi kunde visa att 3DFUS gav valida och reliabla resultat som överensstämde väl med resultaten från MRI undersökningarna. Resultaten visar att 3DFUS kan användas som ett kostnadseffektivt alternativ till MRI för att mäta muskelmorfologi. 

I den andra och tredje studien använde vi två tekniker, magnetisk resonans-elastografi (MRE) och ultraljuds-elastografi (SWE), för att kvantifiera muskulaturens mekaniska egenskaper. Med diffusionstensoravbildning, identifierade vi fascikelns orientering och integrerade denna information i den direkta inversionen av vågekvationen i MRE. Detta tillvägagångssätt möjliggjorde kvantifiering av skelettmuskulaturens anisotropa mekaniska egenskaper antaget att skelettmuskulaturen beter sig som inkompressibelt tvärgående isotropiskt material. Metoden som först valideras med reometrimätningar ex vivo och visade god överensstämmelse mellan MRE och reometrimätningar. Därefter tillämpades mätningen i vivo på mediala gastrocnemius (MG) som också visade god anisotropi. Vi jämförde sedan denna teknik med ett kommersiellt ultraljuds SWE-system, där skelettmuskulaturen antogs vara isotrop. Genom att kvantifiera skjuvvågshastighet från dessa två tekniker visade vi en måttlig till stark korrelation mellan SWE och MRE i ex vivo muskelprover och en stark korrelation mellan dessa två tekniker i MG in vivo. Resultat tyder på att mätningar med det kommersiella ultraljuds SWE-systemet inte signifikant påverkade kvantifieringen av muskelmekaniska egenskaper även med det isotropiska antagandet. 

I den fjärde studien använde vi MRI för att utvärdera eventuella förändringar i vadmuskulaturen avseende morfologiska egenskaper och fettsammansättning 12 månader efter spasticitetsreducerande behandling med botulinumtoxin typ A (BoNT-A) injektioner hos barn med cerebral pares (CP), som inte fått muskeltonsreducerande behandling tidigare. Vi visade att vadmuskeltillväxten inte var försämrad 12 månader efter BoNT-A-injektion, vilket indikeras av ökad absolut muskelvolym och oförändrad normaliserad muskelvolym. Muskeltillväxten omfattades av samtidig fettinfiltration i form av ökning av intramuskulära fett. 

Ultraljuds- och MRI-teknikerna som presenteras i denna avhandling bidrar till ökad kunskap om metoder för kvantifiering av skelettmuskulaturens morfologi och dess mekaniska egenskaper att använda inom biomekaniken. Metoderna bidrar till ny kunskap och utveckling av medicinska avbildningstekniker som kan implementeras i kliniken och användas vid bedömning av muskelfunktion och för utvärdering av rehabiliteringsåtgärder. 

Place, publisher, year, edition, pages
Stockholm: KTH Royal Institute of Technology, 2025. p. xii, 64
Series
TRITA-SCI-FOU ; 2025:17
Keywords
Magnetic resonance imaging, diffusion tensor imaging, magnetic resonance elastography, Dixon method, ultrasonography, three-dimensional freehand ultrasound, shear wave elastography, cerebral palsy, Magnetisk resonanstomografi, diffusionstensoravbildning, magnetisk resonanselastografi, Dixonmetoden, ultraljud, tredimensionell frihandsultraljud, skjuvvågselastografi, cerebral pares
National Category
Medical Imaging Radiology and Medical Imaging
Research subject
Engineering Mechanics
Identifiers
urn:nbn:se:kth:diva-361815 (URN)978-91-8106-246-5 (ISBN)
Public defence
2025-04-25, Kollegiesalen, Brinellvägen 6, Stockholm, 09:00 (English)
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Note

QC 20250331

Available from: 2025-03-31 Created: 2025-03-28 Last updated: 2025-04-01Bibliographically approved

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Wang, ZhongzhengMoreno, RodrigoWang, Ruoli

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