SHORT REPORTS
ASSESSMENT OF MUSCLE STIFFNESS USING A CONTINUOUSLY SCANNING LASER-DOPPLER VIBROMETER MUHAMMAD SALMAN, PhD,1 KARIM G. SABRA, PhD,1 and MINORU SHINOHARA, PhD2 1
School of Mechanical Engineering, Georgia Institute of Technology, 771 Ferst Drive, Atlanta, Georgia 30332-0356 USA School of Applied Physiology, Georgia Institute of Technology, Atlanta, Georgia, USA Accepted 30 December 2013
2
ABSTRACT: Introduction: A stand-alone and low-cost elastography technique has been developed using a single continuously scanning laser Doppler vibrometer. Methods: This elastography technique is used to measure the propagation velocity of surface vibrations over superficial skeletal muscles to assess muscle stiffness. Results: Systematic variations in propagation velocity depending on the contraction level and joint position of the biceps brachii were demonstrated in 10 subjects. Conclusions: This technique may assist clinicians in characterizing muscle stiffness (or tone) changes due to neuromuscular disorders. Muscle Nerve 000:000–000, 2014
Neuromuscular disorders (such as muscular dystrophy and amyotrophic lateral sclerosis) often alter muscle stiffness (or “tone”), thus affecting the patient’s movement capability. Muscle stiffness is most commonly sensed qualitatively with manual palpation in clinical practice.1 Thus, objectively quantifying elastic properties of skeletal muscles may help clinicians to assess therapeutic progress and recovery from muscle disorders. Dynamic elastography methods1 can assess the stiffness of soft tissues by measuring the propagation velocity of induced vibrations, in which faster propagation velocities indicate stiffer tissues. Dynamic elastography methods using magnetic resonance2–5 or ultrafast ultrasound imaging techniques6–9 are available, but their relatively high costs may limit widespread adoption of objective stiffness quantification in clinical settings. Previous studies have demonstrated the use of surface waves for estimating tissue stiffness.10–13 Hence, to explore the development of a simple, noninvasive, in vivo, and more affordable elastography method that may potentially lead to future application in clinical settings, we used surface wave propagation over superficial muscles at many points simultaneously using a single continuously scanning laser Doppler vibrometer (CSLDV).14 The CSLDV allows for simple measurement of the Abbreviations: CSLDV, continuously scanning laser Doppler vibrometer; MVC, maximal voluntary contraction Key words: elastography; laser vibrometry; muscle stiffness; skeletal muscles; surface waves Correspondence to: K. Sabra, e-mail: [email protected] C 2014 Wiley Periodicals, Inc. V
Published online 00 Month 2013 in Wiley Online Library (wileyonlinelibrary. com). DOI 10.1002/mus.24161
Short Reports
velocity of muscle surface waves in a more robust manner when compared with measurements using a single fixed laser beam.14 We investigated the feasibility of this CSLDV-based elastography technique by examining the differences in propagation velocity due to contraction level and joint position. MATERIALS AND METHODS
Ten healthy men (age, 29 6 5 years; height, 175 6 9 cm; body mass, 71 6 8 kg), with apparent various skin and subcutaneous fat thicknesses, without overt sign of neuromuscular diseases were tested. The study was approved by the Institutional Review Board of the Georgia Institute of Technology, and informed consent was obtained before testing. The elbow joint angle was set to 90 with the upper arm laying flat (Fig. 1A). Subjects performed 2 series of 1-s steady isometric contractions with the wrist joint in either neutral (0 deg) or supinated (90 deg) positions. Each series consisted of 3 trials of isometric contractions with elbow flexors at force levels of 0% (rest), 30%, and 60% of maximal voluntary contraction (MVC) in the respective wrist position. The submaximal measurements were made in a randomized order to minimize the potential extraneous effect of fatigue or systematic changes in muscle activation strategy with time. The time interval between submaximal measurements was 20 s or longer. With brief submaximal contractions, the potential effect of the possible development of fatigue was thought to be minimal. Laser elastography measurements were performed for the 10 subjects using the same set-up and procedure described in detail in Salman and Sabra14 and previously validated using soft gel samples. The length Lm of the long head of the biceps brachii muscle was determined based on anatomical landmarks11 such as epicondyle and head of humerus as shown in Figure 1A. A thin rod (8-mm diameter) was placed at a distance 0.44 Lm proximal to the origin of the tendon of insertion and was actuated by an electrodynamic mini-shaker (model 4810, Br€ uel & Kjær, Nærum, Denmark) to generate low-frequency (5–80 HZ) impulses. A computer-controlled fast steering mirror (S-334, MUSCLE & NERVE
Month 2014
1
FIGURE 1. a: Schematic of the experimental set-up. Elbow joint angle was 90 deg, and wrist joint was in neutral (0 deg) or supinated (90 deg) position. b: Velocity of transverse vibrations propagating along the biceps muscle as a function of force level. Mean 6 SD.
Physik Instrumente, Karlsruhe, Germany) continuously deflected the LDV beam (PDV 100, Polytec, Irvine, California) along a 5-cm-long thin retroreflective adhesive tape attached over the biceps belly and centered at a set distance of 0.26 Lm (shown in Fig. 1A). The signal of the CSLDV was finally demultiplexed to measure the average velocity (m/s) of the propagating transverse vibrations along the 5-cm line scan.14 The average velocity of 3 trials in each condition was used for statistical analysis. To test the effect of force level and wrist position on propagation velocity, a 2-factor analysis of variance with repeated measures was performed. An alpha level of 0.05 was used for significance. RESULTS
For each subject and tested contraction level, the measured velocity values varied by 10% at most in the 3 trials, thus indicating fairly good repeatability of the proposed technique given the inherent variability of the testing procedure and force level fluctuations. When the averaged values of 3 trials were compared, there were main effects of force level (P < 0.01) and wrist position (P < 0.05) on the propagation velocity (Fig. 1B). The mean value ranged from 3.83 6 1.26 m/s to 13.02 6 3.21 m/s. For the main effect of force level, the propagation velocity increased from 4.48 6 1.39 m/s at 0% MVC (i.e., at rest) to 9.58 6 2.91 m/s at 30% MVC, and to 12.44 6 3.18 m/s at 60% MVC, when collapsed across wrist positions. For the main effect of wrist position, the propagation velocity in the supinated position (9.50 6 4.16 m/s, collapsed across force levels) was slightly higher compared 2
Short Reports
with the neutral position (8.16 6 4.19 m/s) across contraction levels. There was no significant interaction of contraction level and wrist position. DISCUSSION
The measured velocity values (3.8–13.0 m/s) using this laser-based elastography technique are in quantitative agreement with shear-wave velocities measured for the biceps muscle during similar efforts using either ultrafast ultrasound elastography7 or magnetic resonance elastography15,16 techniques. Relatively high SD compared with the mean at rest may be due, at least in part, to the inherent variability of stiffness of soft tissues, including skin and subcutaneous fat, among tested individuals. The increases in propagation velocity with increases in force level also correspond to findings in various human muscles using other elastography methods.7–9,15,16 As one of the wrist supinators, biceps brachii is slightly activated and its tone is increased with supination of the wrist joint. The higher propagation velocity in the supinated wrist position indicates that laser-based elastography is sensitive enough to detect such a slight increase in muscle stiffness. The proposed technique based on surface wave sensing can only assess superficial muscles, and thus deeper muscles should be investigated using other techniques, such as MRI or ultrasound-based elastography devices. Furthermore, the measured velocity values result from the integrated contribution of the biceps brachii muscle and overlaying skin and fat layers. Based on transient elastography principles1 actual muscle stiffness could be MUSCLE & NERVE
Month 2014
inferred from velocity for a given biomechanical model, but strong simplifying assumptions must be made regarding the mechanical behavior of the tested muscle. Practically speaking, however, measuring relative variations of the velocity may be sufficient to quantify relative changes of the mechanical state of skeletal muscles across various conditions within individuals. As another advantage, laser-based elastography can be performed in near real-time (
ASSESSMENT OF MUSCLE STIFFNESS USING A CONTINUOUSLY SCANNING LASER-DOPPLER VIBROMETER MUHAMMAD SALMAN, PhD,1 KARIM G. SABRA, PhD,1 and MINORU SHINOHARA, PhD2 1
School of Mechanical Engineering, Georgia Institute of Technology, 771 Ferst Drive, Atlanta, Georgia 30332-0356 USA School of Applied Physiology, Georgia Institute of Technology, Atlanta, Georgia, USA Accepted 30 December 2013
2
ABSTRACT: Introduction: A stand-alone and low-cost elastography technique has been developed using a single continuously scanning laser Doppler vibrometer. Methods: This elastography technique is used to measure the propagation velocity of surface vibrations over superficial skeletal muscles to assess muscle stiffness. Results: Systematic variations in propagation velocity depending on the contraction level and joint position of the biceps brachii were demonstrated in 10 subjects. Conclusions: This technique may assist clinicians in characterizing muscle stiffness (or tone) changes due to neuromuscular disorders. Muscle Nerve 000:000–000, 2014
Neuromuscular disorders (such as muscular dystrophy and amyotrophic lateral sclerosis) often alter muscle stiffness (or “tone”), thus affecting the patient’s movement capability. Muscle stiffness is most commonly sensed qualitatively with manual palpation in clinical practice.1 Thus, objectively quantifying elastic properties of skeletal muscles may help clinicians to assess therapeutic progress and recovery from muscle disorders. Dynamic elastography methods1 can assess the stiffness of soft tissues by measuring the propagation velocity of induced vibrations, in which faster propagation velocities indicate stiffer tissues. Dynamic elastography methods using magnetic resonance2–5 or ultrafast ultrasound imaging techniques6–9 are available, but their relatively high costs may limit widespread adoption of objective stiffness quantification in clinical settings. Previous studies have demonstrated the use of surface waves for estimating tissue stiffness.10–13 Hence, to explore the development of a simple, noninvasive, in vivo, and more affordable elastography method that may potentially lead to future application in clinical settings, we used surface wave propagation over superficial muscles at many points simultaneously using a single continuously scanning laser Doppler vibrometer (CSLDV).14 The CSLDV allows for simple measurement of the Abbreviations: CSLDV, continuously scanning laser Doppler vibrometer; MVC, maximal voluntary contraction Key words: elastography; laser vibrometry; muscle stiffness; skeletal muscles; surface waves Correspondence to: K. Sabra, e-mail: [email protected] C 2014 Wiley Periodicals, Inc. V
Published online 00 Month 2013 in Wiley Online Library (wileyonlinelibrary. com). DOI 10.1002/mus.24161
Short Reports
velocity of muscle surface waves in a more robust manner when compared with measurements using a single fixed laser beam.14 We investigated the feasibility of this CSLDV-based elastography technique by examining the differences in propagation velocity due to contraction level and joint position. MATERIALS AND METHODS
Ten healthy men (age, 29 6 5 years; height, 175 6 9 cm; body mass, 71 6 8 kg), with apparent various skin and subcutaneous fat thicknesses, without overt sign of neuromuscular diseases were tested. The study was approved by the Institutional Review Board of the Georgia Institute of Technology, and informed consent was obtained before testing. The elbow joint angle was set to 90 with the upper arm laying flat (Fig. 1A). Subjects performed 2 series of 1-s steady isometric contractions with the wrist joint in either neutral (0 deg) or supinated (90 deg) positions. Each series consisted of 3 trials of isometric contractions with elbow flexors at force levels of 0% (rest), 30%, and 60% of maximal voluntary contraction (MVC) in the respective wrist position. The submaximal measurements were made in a randomized order to minimize the potential extraneous effect of fatigue or systematic changes in muscle activation strategy with time. The time interval between submaximal measurements was 20 s or longer. With brief submaximal contractions, the potential effect of the possible development of fatigue was thought to be minimal. Laser elastography measurements were performed for the 10 subjects using the same set-up and procedure described in detail in Salman and Sabra14 and previously validated using soft gel samples. The length Lm of the long head of the biceps brachii muscle was determined based on anatomical landmarks11 such as epicondyle and head of humerus as shown in Figure 1A. A thin rod (8-mm diameter) was placed at a distance 0.44 Lm proximal to the origin of the tendon of insertion and was actuated by an electrodynamic mini-shaker (model 4810, Br€ uel & Kjær, Nærum, Denmark) to generate low-frequency (5–80 HZ) impulses. A computer-controlled fast steering mirror (S-334, MUSCLE & NERVE
Month 2014
1
FIGURE 1. a: Schematic of the experimental set-up. Elbow joint angle was 90 deg, and wrist joint was in neutral (0 deg) or supinated (90 deg) position. b: Velocity of transverse vibrations propagating along the biceps muscle as a function of force level. Mean 6 SD.
Physik Instrumente, Karlsruhe, Germany) continuously deflected the LDV beam (PDV 100, Polytec, Irvine, California) along a 5-cm-long thin retroreflective adhesive tape attached over the biceps belly and centered at a set distance of 0.26 Lm (shown in Fig. 1A). The signal of the CSLDV was finally demultiplexed to measure the average velocity (m/s) of the propagating transverse vibrations along the 5-cm line scan.14 The average velocity of 3 trials in each condition was used for statistical analysis. To test the effect of force level and wrist position on propagation velocity, a 2-factor analysis of variance with repeated measures was performed. An alpha level of 0.05 was used for significance. RESULTS
For each subject and tested contraction level, the measured velocity values varied by 10% at most in the 3 trials, thus indicating fairly good repeatability of the proposed technique given the inherent variability of the testing procedure and force level fluctuations. When the averaged values of 3 trials were compared, there were main effects of force level (P < 0.01) and wrist position (P < 0.05) on the propagation velocity (Fig. 1B). The mean value ranged from 3.83 6 1.26 m/s to 13.02 6 3.21 m/s. For the main effect of force level, the propagation velocity increased from 4.48 6 1.39 m/s at 0% MVC (i.e., at rest) to 9.58 6 2.91 m/s at 30% MVC, and to 12.44 6 3.18 m/s at 60% MVC, when collapsed across wrist positions. For the main effect of wrist position, the propagation velocity in the supinated position (9.50 6 4.16 m/s, collapsed across force levels) was slightly higher compared 2
Short Reports
with the neutral position (8.16 6 4.19 m/s) across contraction levels. There was no significant interaction of contraction level and wrist position. DISCUSSION
The measured velocity values (3.8–13.0 m/s) using this laser-based elastography technique are in quantitative agreement with shear-wave velocities measured for the biceps muscle during similar efforts using either ultrafast ultrasound elastography7 or magnetic resonance elastography15,16 techniques. Relatively high SD compared with the mean at rest may be due, at least in part, to the inherent variability of stiffness of soft tissues, including skin and subcutaneous fat, among tested individuals. The increases in propagation velocity with increases in force level also correspond to findings in various human muscles using other elastography methods.7–9,15,16 As one of the wrist supinators, biceps brachii is slightly activated and its tone is increased with supination of the wrist joint. The higher propagation velocity in the supinated wrist position indicates that laser-based elastography is sensitive enough to detect such a slight increase in muscle stiffness. The proposed technique based on surface wave sensing can only assess superficial muscles, and thus deeper muscles should be investigated using other techniques, such as MRI or ultrasound-based elastography devices. Furthermore, the measured velocity values result from the integrated contribution of the biceps brachii muscle and overlaying skin and fat layers. Based on transient elastography principles1 actual muscle stiffness could be MUSCLE & NERVE
Month 2014
inferred from velocity for a given biomechanical model, but strong simplifying assumptions must be made regarding the mechanical behavior of the tested muscle. Practically speaking, however, measuring relative variations of the velocity may be sufficient to quantify relative changes of the mechanical state of skeletal muscles across various conditions within individuals. As another advantage, laser-based elastography can be performed in near real-time (
