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Analysis of thigh muscle stiffness from childhood to adulthood using magneticresonance elastography (MRE) technique

Laëtitia Debernard a, Ludovic Robert b, Fabrice Charleux b, Sabine F. Bensamoun a,⁎a Biomechanics and Bioengineery Laboratory, UMR CNRS 6600, Université de Technologie de Compiègne, Compiègne, Franceb ACRIM-Polyclinique Saint Côme, Compiègne, France

a b s t r a c ta r t i c l e i n f o

Article history:Received 22 September 2010Accepted 13 April 2011

Keywords:Shear modulus mapAgeMuscle growthMagnetic resonance elastography

Background: Magnetic resonance elastography has been performed in healthy and pathological muscles inorder to provide clinicians with quantitative muscle stiffness data. However, there is a lack of data on pediatricmuscle. Therefore, the present work studies age-related changes of the mechanical properties.Methods: 26 healthy subjects composed of 7 children (8–12 years), 9 young adults (24–29 years) and 10middle-aged adults (53–58 years) underwent amagnetic resonance elastography test. Shear modulus (μ) andits spatial distribution, as well as the attenuation coefficient (α) weremeasured on the vastus medialis muscleat rest and at contracted conditions (10% and 20% of the maximum voluntary contraction) for each group.Findings: The shear modulus linearly increases with the degree of contraction for young adults while it ismaximum at 10% of the maximum voluntary contraction for children (μ_children_10%=14.9 kPa (SD 2.18)) andmiddle-aged adults (μ_middle-aged_10%=10.42 kPa (SD 1.38)). Mapping of shear modulus revealed a diffusedistribution of colors reflecting differences inmuscle physiological activity as a function of age. The attenuationcoefficient showed a similar behavior for all groups, i.e. a decrease from the relaxed to the contracted states.Interpretation: This study demonstrates that the magnetic resonance elastography technique is sensitiveenough to detect changes in muscle mechanical properties for children, middle-aged and young adults andcould provide clinicians with a muscle reference data base as a function of age, improving the diagnosis ofmuscular dystrophy.

© 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Muscle pathologies such as myopathy detected in childhood,fibromyalgia present in adult muscles or muscle weakness exhibitedby older individuals can alter the muscle's stiffness and its morpholog-ical properties. As a consequence of the morphological changes, themechanical properties of muscle are also affected. Most of the studies(e.g. Akima et al., 2001; Lynch et al., 1999) used an isokinetic dynamo-meter to measure peak torque during knee extension and flexion, orconcentric and eccentric elbow movements. All of these analysesshowed a gradual decrease of the mechanical parameters, for men andwomen aged between 20 and 85 years. Since 2001,magnetic resonanceelastography (MRE) technique has also been used to characterize in vivomechanical properties of healthy and diseased muscle (Basford et al.,2002; Bensamoun et al., 2006, 2007; Brauck et al., 2007; Dresner et al.,2001). This technique analyzed the propagation of shear waves insidethe muscle allowing for the measurement of shear modulus which is

related to the muscle function. Indeed, the magnetic resonance elasto-graphy was performed on patients with lower-extremity neuromuscu-lar dysfunction (Basford et al., 2002), hyperthyroidy (Bensamoun et al.,2007) and fibromalgia (Chen et al., 2007, 2008) in order to establish amuscle's stiffness data base for the follow up of patient and the effect oftreatment. Furthermore, Domire et al. (2009a) have analyzed thestandard deviation of the shearmodulus to investigate themuscle tissuehomogeneity and a relationship was found between the age (50 to70 years) and the tissue homogeneity for the tibialis anterior muscle. Inaddition to the shear modulus, magnetic resonance elastography canprovide a wave attenuation coefficient as a measure of muscle quality(Domire et al., 2009b).

Most of themuscle MRE studies were performed on adults' muscles,aged between 20 and 80 years, but there is a lack of data characterizingthemechanical properties ofmuscle for children. Indeed,morphologicalproperties were widely quantified by ultrasound studies on healthychildren showing relevant changes in echogenicity (Kamala et al., 1985;Lamminen et al., 1988; Pillen et al., 2007; Zuberi et al., 1999), musclearchitecture (Debernard et al., 2011), muscle and subcutaneousadipose tissue thicknesses (Heckmatt et al., 1988; Zuberi et al., 1999).This study is the first to show the capability of the magnetic resonanceelastography technique to measure muscle's stiffness in children andcould provide clinicians with a muscle reference data base for healthy

Clinical Biomechanics 26 (2011) 836–840

⁎ Corresponding author at: Université de Technologie de Compiègne (UTC), Centrede Recherches de Royallieu, Laboratoire de Biomécanique et Bioingénierie, UMR CNRS6600, BP 20529, Rue Personne de Roberval, 60205 Compiègne cedex, France.

E-mail address: sabine.bensamoun@utc.fr (S.F. Bensamoun).

0268-0033/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.doi:10.1016/j.clinbiomech.2011.04.004

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pediatric muscles which could be compared with those of childrenaffected by neuromuscular disorders.

The purpose of this study is to characterize the vastus medialismechanical properties at different muscle conditions for children,young adults and middle-aged adults. Moreover, the originality of thepresent study was to show the changes in the shear modulus map as aresult of level of muscle contraction.

2. Methods

2.1. Participants

Seven prepubescent children (6 males and 1 female, mean age=10.9 yrs (SD 0.6), range=8–12, mean bodymass index 17.3 (SD 0.9)),nine young adults (5 males and 4 females, mean age=26.4 yrs(SD 1.7), range=24–29, mean body mass index 23.69 (SD 3.34)) andten middle-aged adults (3 males and 7 females, mean age=55.2 yrs(SD 2.39), range=52–58, mean body mass index 26.39 (SD 4.72))without muscle abnormality and no history of muscle diseaseunderwent a magnetic resonance elastography test. These threeage points have been chosen to represent different muscle statescorresponding to the muscle growing phase (child), a mature muscle(young adult) and the first beginning of aging muscle (middle-agedadult). This study has been approved by the institutional review boardand informed consents were obtained from adult participants andfrom the parents for minor volunteers.

2.2. Experimental setup for magnetic resonance elastography technique

The subject lays supine on an adult leg press (Bensamoun et al.,2006) which, when used for children, was adapted for the child's size.The knee was flexed to 30° with the right foot placed on a footplate, inwhich a load cell (SCAIME, Annemasse, France) was fixed to recordthe developed force and a visual feedback (LABVIEW program) of theapplied load is given to the volunteers inside the magnetic resonanceroom. Then, a pneumatic driver consisting of a remote pressure driverconnected to a long hose was wrapped and clamped around thesubject's thigh and a custom-made Helmholtz surface coil was placedaround the thigh. Shear waves were induced through the thighmuscles at 90 Hz (f).

Magnetic resonance elastography experiments were performedfor each subject on the vastus medialis muscle, in the relaxed andcontracted (10% and 20% of the maximum voluntary contraction)states. A delay of 5 min between individual experiments was given tothe volunteers in order to avoid fatigue effects. Repeatability of theMRE test was done twice on two subjects, at each age point, when themuscle was relaxed and contracted.

2.3. Magnetic resonance elastography tests

Axial image of the thigh muscle was acquired with a gradient echosequence (1.5 TGeneral ElectricHDxtMRI) in order to place an obliquescan plane on the medial side of the thigh to visualize the vastusmedialis muscle. Then, magnetic resonance elastography imageswere collected with a 256×64 acquisition matrix (interpolated to256×256), aflip angle of 45°, a 24 cmfield of viewand a slice thicknessof 5 mm. Four offsets were recorded with the vastus medialis musclein relaxed and contracted (10%, 20% MVC) states during a scan timeof 52 seconds using a repetition time and a echo time of 100 ms and23 ms, respectively.

2.4. Image processing and data analysis

Magnetic Resonance elastography provides an anatomical image ofthe vastus medialis muscle (Fig. 1a) as well as phase image (Fig. 1b)showing the shear wave displacement within the muscle. A whiteprofile was manually placed in the direction of the wave propagationthat follows the orientation of the fascicle paths as previouslydemonstrated (Debernard et al., 2011). The quantification of thewavelength (λ) along this profile leads to the measurement of thelocal shear modulus (μ_local=ρλ2f2, with ρ=1000 kg/m3 for themuscle density) assuming that the muscle is linearly elastic, locallyhomogeneous, isotropic and incompressible.

Attenuation coefficient (α) of the shear wave amplitude wasmeasured along the prescribed white profile. This parameter isobtained from a Fourier Transform of the distance covered by eachpixel during the four offsets (Domire et al., 2009b). The amplitudevalue of the first temporal harmonic of each pixel was extracted at thedriven frequency, 90 Hz, providing the amplitude image (Fig. 1c).Then a curve of shear wave amplitude along the profile (samplingstep corresponding to the pixel size: 0.9 mm) was obtained and fittedwith an exponential function Ae−(αd), with the parameters “A” and“d” representing the displacement amplitude value and the distancealong the profile, respectively (Fig. 2).

A map of the shear modulus was generated from the wavedisplacement image using the local frequency estimation algorithm(Manduca et al., 2001) providing a spatial distribution of the muscleshear modulus. Assuming that muscle tissue is locally homogeneous,an ellipsoid region of interest was placed around the prescribedprofile in order to quantify the shear modulus of a larger muscle areareferred to the global shear modulus (μ_ROI). Thus, not only a localshear modulus (μ_local) was measured but also a global shearmodulus (μ_ROI), and both measurements were compared to validatethe global shear modulus value obtained through the magneticresonance elastography cartography.

Fig. 1. A: anatomical image of the vastus medialis (VM) muscle in a relaxed state. B: Phase image with a white profile drawn along the direction of the shear wave's propagationfollowing the path of muscle fascicle. C: Amplitude image resulting from the amplitude value of the first temporal harmonic extracted at the driven frequency 90 Hz along each pixel.

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2.5. Statistical analysis

The statistical analysis was performed with the software Statgraphics5.0 (SigmaPlus,Maryland, USA) using a two-factor ANOVA (age,musclestate) and when P values were significant post hoc t-test (Student–Newman–Keuls) were done. The effects of age and level of contractionwere determined on shear modulus and attenuation coefficient. Thesignificance was fixed to Pb0.05.

3. Results

3.1. Effect of muscle condition (relaxed or contracted) on local shearmodulus (μ_local) and attenuation coefficient (α) for children, young adultsand middle-aged adults.

Young adults showed a significant (Pb0.05) linear increase of theshearmodulus from the relaxed to 20%MVC,whereas children and olderindividuals showed only a significant (Pb0.05) increase between therelaxed and10%MVC(Fig. 3, Table 1).Wenote that children revealed the

highest increase of shear modulus (5 fold) from the relaxed to thecontracted (10%MVC) state (Fig. 3),whereas theyoungandmiddle-agedadults showed a lower increase of muscle shear modulus (about 2 fold)(Fig. 3, Table 1). Between 10% and 20% MVC, individuals in their fiftiesrevealed a slight decrease (Fig. 3), compared to the young adults whocontinue to increase their shear modulus with the same ratio (2 fold)(Fig. 3).

The repeatability of the MRE test was about 0.3 kPa and 0.6 kPa forrelaxed and contracted muscle conditions, respectively, across agegroups. Moreover, the reproducibility of the shear modulus wasmeasured as the standard deviation (SD) from successive magneticresonance elastography tests with a delay of 5 min between each test.Reproducibility of the shear modulus was 0.25 kPa at rest while incontraction the measurements were 2.66 kPa, 1.12 kPa and 1.56 kPafor children, young adults and middle-aged adults, respectively.

The effect of the muscle condition (relaxed or contracted) on theshear wave attenuation was the same for the three age groups. Thus,children, young andmiddle-aged adults showed a significant (Pb0.05)decrease of 34.72 m−1 (SD 3.13), 18.75 m−1 (SD 0.93) and 12.00 m−1

(SD 1.64) between the relaxed state and 10% of MVC, respectively(Fig. 4, Table 2). In agreementwith the shearmodulus results, childrenshowed the largest change in attenuation between the relaxed and10% MVC condition. Then, the attenuation coefficient is consistentlymaintained from 10% to 20% of MVC for all the groups (Fig.4).

3.2. Effect of age on the muscle local shear modulus (μ_local) andattenuation coefficient (α) for the relaxed and contracted positions

In a relaxed state, the children had a slightly significant (Pb0.05)lower shear modulus (μ_children=2.99 kPa (SD 0.19)) compared toadults' groups which have similar shear modulus (μ_young=3.83 kPa(SD 0.24), μ_middle-aged=3.84 kPa (SD 0.42)) (Fig. 3, Table 1).

At 10% of MVC, the highest significant difference (Pb0.05) of shearmodulus was found between children and young adults (about 7.6 kPa)while a smaller differencewas found between the adults' groups (about3 kPa). However, no difference was found between children andmiddle-aged adults, probably due to the large range of shear modulusmeasured for children. At 20% of MVC, only a significant (Pb0.05)difference of shear modulus was found between adult's groups.

The only effect of age on the shear wave attenuation was foundwhenthe muscle was relaxed (Fig. 4). Indeed, children revealed a significant(Pb0.05) difference with young adults (about 13 m−1) (Fig. 4). Theresultsdonotdemonstrateanyeffect of ageon the shearwaveattenuationwhen the muscle was contracted.

3.3. Cartography of muscle stiffness reflecting the global shearmodulus (μ_ROI)

Fig. 5 illustrates the shear modulus map and the correspondinganatomical image obtained for the children, young and middle-agedsubjects when the vastus medialis muscle was at rest and contractedto 10% and 20% of MVC. At rest, we observed that the shear modulusmap for the three groups revealed a homogeneous purple color in theregion of interest (ROI) (Fig. 5a, d, and g) placed around the red profilewhere the shear modulus was locally quantified. The comparison ofthe shear modulus measured inside the region of interest and alongthe red profile was in the same range (Table 1).

When the vastus medialis muscle was contracted, the shearmodulus map exhibited a diffuse change of colors, throughout theregion of interest (Fig. 5b–c,e–f, and h–i), demonstrating that theshear waves were sensitive to the muscle media and morespecifically to the contraction of the muscle fibers. At 10% MVC,children showed the highest shear modulus value locally measuredalong the profile, and similarly the shear modulus map (μ_local=14.9(SD 2.02) vs. μ_ROI=12.4 (SD 1.36)) revealed stiffer tissues inside theregion of interest (Fig. 5b, Table 1) in response to the muscle

Fig. 3. Bar graph of the local shearmodulus (μ_local) measured along the propagation of theshearwaves for each age points and for different VMmuscle conditions (rest, 10% and 20%of the maximum voluntary contraction, MVC) (** Pb0.05).

Fig. 2. Computation of the attenuation coefficientα (m−1) from the wave displacementamplitude in function of the distance.

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contraction. For the same level of contraction (10% MVC) stiffermuscle tissue showed up inside the region of interest for children(Fig. 5b, Table 1) compared to adult's groups (Fig. 5e–h). Moreover,this result is in agreement with the highest shear modulus measuredlocally along the white profile for children compared to adult groups.At 20% MVC, young adults (Fig.5f) exhibited stiffer muscle tissuearound the region of interest compared to the mapping obtainedat 10% MVC (Fig. 5e). This result is in agreement with the linearincrease of shear modulus previously found between 10% and 20%MVC. At the opposite, middle-aged participants showed a mappingwith less stiff tissue around the region of interest at 20% MVC(μ_ROI=8.53 kPa (SD 2.01)) (Fig. 5i) than 10% MVC (μ_ROI=10.7 kPa(SD 2.06)) (Fig. 5h), confirming the slight decrease of the shearmodulus locally measured at 10% and 20% MVC.

4. Discussion

The increaseof themuscle shearmoduluswith the level of contractionis in agreementwith the literature (Basford et al., 2002; Bensamoun et al.,2006; Dresner et al., 2001). Slight differences in values may exist due toeither the experimental set up (pneumatic vs. mechanical driver) or thechoice of frequency (90 Hz vs. 120 Hz). Moreover, MRE experimentsrevealed an interaction between the age, muscle states and mechanicalproperties. Indeed, at 10% MVC, individuals in their fifties and childrenhave already reached a maximal shear modulus compared to youngadults that realize progressive muscle fiber recruitment according to thedegree of contraction (Bensamounet al., 2006). Thepresent study revealsthat persons in their fifties required an important fiber recruitment toreach a small level of contraction (10% MVC). Thus at this level ofcontraction, the massive fiber recruitment may explain the difference

(about 3 kPa) in the shear modulus between young and middle-agedsubjects.

Children showed a significant lower shearmodulus at rest comparedto the adult's groups which have similar muscle stiffness. This resultdemonstrated the capability of the shear wave to reflect different age-related muscle media. According to the present results, it is apparentthat muscle structure is different in children, while it is the same foradults aged between 20 and 59 years. Similar results were found byDomire et al. (2009a), i.e. no significant difference of shear modulusmeasured at rest for the tibialis anteriormuscle for adults aged between50 and 70 years. This last result is surprising because at this age, themuscle has already undergone the aging process that could have alteredthe muscle mechanical properties. However, the effect of age may notaffect in the sameway all skeletalmuscles of the lower and upper limbs.In addition, the physical condition may also explain the large range ofshear modulus found in elderly people. For a small level of contraction(10% MVC) children demonstrated the highest shear modulus valuescompared to adult's groups. Indeed, during the muscle maturationprocess there is an on-going structural organization with the lengthen-ing of the fiber, leading to random and uncontrolled fiber recruitment(Debernard et al., 2011). As a consequence, pediatricmusclewas unableto control progressively muscle fiber recruitment to perform a smallcontraction, and instead contract unintentionally all the muscle fibersleading to a high shear modulus. Over activation of the muscle at lowactivities (b25% of MVC) was also found in the literature for the tricepssurae muscle of children (7 to 11 years old) (Grosset et al., 2008).

The attenuation coefficient is a mechanical parameter reflecting themuscle quality (Domire et al., 2009b) and the ones obtained in this studyfor relaxedmusclewere in the same range as those found in the literaturefor the samemuscle (Domire et al., 2009b). Toour knowledge, thepresentwork provides the first database of attenuation coefficients for activemuscle. According to the present results, it can be stated that theattenuationcoefficientdecreasedasa result ofmuscle contraction. Indeed,this last result could be used as an additional mechanical parameter forthe characterization of pathological muscles.

This present study is the first to measure muscle shear modulusin children through the use of magnetic resonance elastographytechnique and to study changes of the mechanical properties forchildren, young andmiddle-aged adults. The originality of the presentstudy was to show the changes in the shear modulus map as a resultof level of muscle contraction. Indeed, the mappings obtained atrest, 10% MVC and 20% MVC provide information about the spatialdistribution of the contracted muscle area related to the physiologicalactivity or other intrinsic muscle parameters such as the degree of themuscle fibers orientation, the tension of muscle fibers or connective

Table 1Table of the comparison of the shear modulus measured locally (μ_local) and inside the region of interest (μ_ROI) for the vastus medialis muscle of children, young and middle-agedadults at rest and contracted states (10% and 20% of the maximum voluntary contraction, MVC).

REST 10%MVC 20%MVC

μ_local (kPa) μ_ROI (kPa) μ_local (kPa) μ_ROI (kPa) μ_local (kPa) μ_ROI (kPa)

Children 2.99 (SD 0.19) 3.61 (SD 0.27) 14.9 (SD 2.18) 12.4 (SD 1.36) 15.05 (SD 2.73) 13.3 (SD 2.03)Young adults 3.83 (SD 0.24) 4.14 (SD 0.26) 7.33 (SD 1.23) 7.46 (SD 0.85) 12.97 (SD 0.87) 11.9 (SD 1.38)Middle-aged adults 3.84 (SD 0.42) 3.2 (SD 0.48) 10.42 (SD 1.38) 10.7 (SD 2.08) 9.12 (SD 1.19) 8.53 (SD 2.01)

Fig. 4. Bar graph illustrating the attenuation coefficient (α) in relaxed and contracted(10% and 20% of the maximum voluntary contraction, MVC) states for children, youngand middle-aged adults ( ** Pb0.05).

Table 2Table of the attenuation coefficient (α) in relaxed and contracted (10% and 20% of themaximum voluntary contraction, MVC) states for children, young and middle-agedadults.

Attenuation coefficient (m−1)

REST 10%MVC 20%MVC

Children 59.43 (SD 7.44) 24.71 (SD 4.31) 23.17 (SD 4.91)Young adults 46.89 (SD 6.35) 28.14 (SD 5.42) 21 (SD 2.13)Middle-aged adults 41.2 (SD 5.68) 29.2 (SD 7.37) 24 (SD 3.93)

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tissue as well as the environmental muscle tissues. Stiffnesses imageswere also presented by Chen at al. (2007, 2008) for upper trapeziusmuscle affected bymyofascial pain in order to visualize and to localizeareas of higher stiffness.

5. Conclusion

In conclusion, this study demonstrates that the magnetic resonanceelastography technique is sensitive enough to detect changes inmusclephysiological activity properties in children, young and middle-agedadults. It would be of interest to study the gender distribution as afunctionof age and toextend this studyatdifferent agepoints in order toaccurately follow changes occurring during the muscle maturation andaging process. Furthermore, the characterization of the mechanicalproperties for normal children will provide clinicians with a muscles'stiffness database in order to quantitatively assess pathological musclesand the effects of treatments and therapies.

Acknowledgments

This work was supported by the Foundation Motrice and thePicardie Region.

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Fig. 5.Mapping of shear modulus for the vastusmedialis at rest and contracted (10% and 20% ofMVC) conditions for the children, young andmiddle-aged adults. Muscle stiffness wasanalysed inside the prescribed region of interest defined by a black circle, placed around the red profile for each group and each muscle state.

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