Ultrasound Elastography: The New Frontier in Direct Measurement of Muscle Stiffness

doi:10.1016/j.apmr.2014.07.007

Archives of Physical Medicine and Rehabilitation

Volume 95, Issue 11, November 2014, Pages 2207-2219

https://doi.org/10.1016/j.apmr.2014.07.007 Get rights and content

Abstract

The use of brightness-mode ultrasound and Doppler ultrasound in physical medicine and rehabilitation has increased dramatically. The continuing evolution of ultrasound technology has also produced ultrasound elastography, a cutting-edge technology that can directly measure the mechanical properties of tissue, including muscle stiffness. Its real-time and direct measurements of muscle stiffness can aid the diagnosis and rehabilitation of acute musculoskeletal injuries and chronic myofascial pain. It can also help monitor outcomes of interventions affecting muscle in neuromuscular and musculoskeletal diseases, and it can better inform the functional prognosis. This technology has implications for even broader use of ultrasound in physical medicine and rehabilitation practice, but more knowledge about its uses and limitations is essential to its appropriate clinical implementation. In this review, we describe different ultrasound elastography techniques for studying muscle stiffness, including strain elastography, acoustic radiation force impulse imaging, and shear-wave elastography. We discuss the basic principles of these techniques, including the strengths and limitations of their measurement capabilities. We review the current muscle research, discuss physiatric clinical applications of these techniques, and note directions for future research.

Section snippets

Ultrasound elastography principles and techniques

In general, all methods-testing techniques for determining the material properties of tissue, including mechanical properties, involve measurements of deformation in response to applied stress or force. Ultrasound elastography relies on the same principle. The stress can be produced by internal physiological motions (eg, beating of the heart,18, 19 pulsation of a blood vessel²⁰), external mechanical compression or vibration,21, 22, 23 or a high-intensity long-duration (hundreds of ultrasound

Ultrasound elastography and muscle

Both passive and active muscle stiffness contribute to physical function. The measurement of passive and active stiffness of individual muscles is challenging because common techniques used for musculoskeletal measurements are not capable of measuring individual muscles in isolation. These techniques are gross measurements of the entire joint, muscle, tendon, or neurovascular complex. However, certain conditions (eg, muscular dystrophy, collagen disorders, cerebral palsy, prolonged bed rest,

Future directions

The real-time, direct measurement of the passive and active properties of individual muscles has already begun to advance our basic understanding of skeletal muscle. Improvements in the rehabilitation of patients with these conditions can be expected with greater understanding of the relation between muscle properties and physical function. As this technology and these muscle measurements are being explored, questions remain regarding the measurement capabilities of ultrasound elastography. How

Conclusions

As ultrasound elastography evolves, we must strive to understand its varied techniques, including its strengths, limitations, and anticipated clinical applications for use in muscle measurements. Ultrasound elastography provides the opportunity to further our understanding of the interaction between muscle structure and function by its measurement of individual muscle mechanical properties. Direct measurement has the potential to quantify previously subjective clinical examination measurements

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Mechanical assessments of skeletal muscles have profound relevance in the clinical diagnosis, management, and treatment of neuromuscular diseases. Current clinical measures of muscular biomechanics involve either non-instrumental methods that are subjective and qualitative or bulky instruments with limited accessibility. Here, we develop a wearable device that integrates a pneumatic actuator and a piezoelectric sensor for in vivo measurements of muscular elasticity, where machine learning models are adopted to evaluate the severity of neuromuscular diseases. The wearable conforms to the human body and couples mechano-electrically with the underlying tissues, thereby correlating their elastic moduli with the sensor’s voltage output. Clinical validation was performed on both normative and spastic biceps muscle. Quasi-static tests measure the effective moduli of the muscles, while dynamic tests continuously monitor the modulus change in biceps muscle during rapid joint stretches. This work establishes a new paradigm for remote diagnosis and tele-rehabilitation of muscle-related pathophysiological conditions.
Chinese Ultrasound Doctors Association Guideline on Operational Standards for 2-D Shear Wave Elastography Examination of Musculoskeletal Tissues
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The Ultrasound Physician Branch of the Chinese Medical Doctor Association sought to develop evidence-based recommendations on the operational standards for 2-D shear wave elastography examination of musculoskeletal tissues. A consensus panel of 22 Chinese musculoskeletal ultrasound experts reviewed current scientific evidence and proposed a set of 12 recommendations for 13 key issues, including instruments, operating methods, influencing factors and image interpretation. A final consensus was reached through discussion and voting. On the basis of research evidence and expert opinions, the strength of recommendation for each proposition was assessed using a visual analog scale, while further emphasizing the best available evidence during the question-and-answer session. These expert consensus guidelines encourage facilitation of the standardization of clinical practices for collecting and reporting shear wave elastography data.
Explorative study using ultrasound time-harmonic elastography for stiffness-based quantification of skeletal muscle function
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Time-harmonic elastography (THE) is an emerging ultrasound imaging technique that allows full-field mapping of the stiffness of deep biological tissues. THE's unique ability to rapidly capture stiffness in multiple tissues has never been applied for imaging skeletal muscle. Therefore, we addressed the lack of data on temporal changes in skeletal muscle stiffness while simultaneously covering stiffness of different muscles.
Acquiring repeated THE scans every five seconds we quantified shear-wave speed (SWS) as a marker of stiffness of the long head (LHB) and short head (SHB) of biceps brachii and of the brachialis muscle (B) in ten healthy volunteers. SWS was continuously acquired during a 3-min isometric preloading phase, a 3-min loading phase with different weights (4, 8, and 12 kg), and a 9-min postloading phase. In addition, we analyzed temporal SWS standard deviation (SD) as a marker of muscle contraction regulation.
Our results (median [min, max]) showed both SWS at preloading (LHB: 1.04 [0.94, 1.12] m/s, SHB: 0.86 [0.78, 0.94] m/s, B: 0.96 [0.87, 1.09] m/s, p < 0.001) and the increase in SWS with loading weight to be muscle-specific (LHB: 0.010 [0.002, 0.019] m/s/kg, SHB: 0.022 [0.017, 0.042] m/s/kg, B: 0.039 [0.019, 0.062] m/s/kg, p < 0.001). Additionally, SWS during loading increased continuously over time by 0.022 [0.004, 0.051] m/s/min (p < 0.01). Using an exponential decay model, we found an average relaxation time of 27 seconds during postloading. Analogously, SWS SD at preloading was also muscle-specific (LHB: 0.018 [0.011, 0.029] m/s, SHB: 0.021 [0.015, 0.027] m/s, B: 0.024 [0.018, 0.037] m/s, p < 0.05) and increased by 0.005 [0.003, 0.008] m/s/kg (p < 0.01) with loading. SWS SD did not change over loading time and decreased immediately in the postloading phase.
Taken together, THE of skeletal muscle is a promising imaging technique for in vivo quantification of stiffness and stiffness changes in multiple muscle groups within seconds. Both the magnitude of stiffness changes and their temporal variation during isometric exercise may reflect the functional status of skeletal muscle and provide additional information to the morphological measures obtained by conventional imaging modalities.
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This study examined the effects of ultrasound transducer pressure and examiner experience on the biceps femoris long head and semitendinosus muscle active shear modulus in healthy individuals (n = 28).
Active shear modulus was assessed using shear wave elastography at 20% of knee flexor maximal voluntary isometric contraction. Examiners with different experience levels measured the muscles' shear modulus with three pressure levels: mild, moderate, and hard.
A main effect of transducer pressure was found for both biceps femoris long head (p < 0.001; η²_p = 0.314) and semitendinosus muscles (p < 0.001; η²_p = 0.280), whereas differences were found between mild-moderate (biceps femoris long head: p = 0.013, d = 0.23; semitendinosus: p = 0.024, d = 0.25), and mild-hard pressures (biceps femoris long head: p = 0.001, d = 0.47; semitendinosus: p = 0.002, d = 0.47). Examiners performed similar shear modulus measurements in the biceps femoris long head (p = 0.299; η²_p = 0.041) and semitendinosus (p = 0.177; η²_p = 0.066), although the experienced examiner showed a higher measurement repeatability (biceps femoris long head: ICC = 0.86–0.95, semitendinosus: ICC = 0.89–0.96; vs. biceps femoris long head: ICC = 0.78–0.87, semitendinosus: ICC = 0.66–0.87).
Transducer pressure influences the active shear modulus measurement between mild and moderate or hard pressures. Additionally, examiner experience seems to have no influence on muscle active shear modulus measurement when assessed at the same site (using casts).
Future studies assessing active muscle shear modulus should use mild transducer pressure and having experienced examiners in order to improve measurement reliability.
Reliability of lower leg muscle elasticity using shear wave elastography in non-weight-bearing and weight-bearing
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Muscle elasticity can be quantified with shear wave elastography (SWE) and has been used as an estimate of muscle force but reliability has not been established for lower leg muscles. The purpose of this study was to examine the intra-rater and inter-rater reliability of elasticity measures in non-weight-bearing (NWB) and weight-bearing (WB) for the tibialis anterior (TA), tibialis posterior (TP), peroneal longus (PL), and peroneal brevis (PB) muscles using SWE.
A total of 109 recreationally active healthy adults participated. The study employed a single-cohort, same-day repeated-measures test–retest design. Elasticity, measured in kilopascals as the Young’s modulus, was converted to the shear modulus. All four muscles were measured in NWB and at 90% WB.
Intra-rater reliability estimates were good to excellent for NWB (ICC = 0.930–0.988) and WB (ICC = 0.877–0.978) measures. Inter-rater reliability estimates were moderate to good (ICC = 0.500–0.795) for NWB measures and poor to good (ICC = 0.346–0.910) for WB measures.
Despite the studies poor to good inter-rater variability, the intra-rater reproducibility represents the potential benefit of SWE in NWB and WB. Establishing the reliability of SWE with clinical and biomechanical approaches may aid in improved understanding of the mechanical properties of muscle.

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: Supported in part by the National Institutes of Health (grant no. KL2TR000136-07); Department of Physical Medicine and Rehabilitation at Mayo Clinic, Rochester, Minnesota; and National Institutes of Health through grants from the National Institute on Aging (grant no. F30 AG044075) and National Institute of General Medical Sciences (grant no. T32 GM 65841).

: Disclosures: Zhao, Chen, and Song disclose royalties from General Electric Medical Systems and Samsung Electronics Company Ltd for ultrasound elastography technology. Chen receives consultation fees from Sonoscape Inc. The authors disclose the following patents: Zhao and Chen: System and Method for Correcting Errors in Shear Wave Measurements Arising from Ultrasound Beam Geometry (patent no. 8,734,350); Chen: Vibration Generation and Detection in Shear Wave Dispersion Ultrasound Vibrometry with Large Background Motions (patent no. 8,659,975), Method for Ultrasound Vibrometry using Orthogonal Basis Functions (patent no. 8,602,994), Detection of Motion in Vibro-Acoustography (patent no. 7,785,259), Ultrasound Vibrometry (patent no. 7,753,847), Method and Apparatus for Shear Property Characterization from Resonance Induced by Oscillatory Radiation Force (patent no. 7,713,201); An: Expandable Screw Apparatus and Method (patent no. 6,668,688), Spinal Fixation Support Device and Methods of Using (patent no. 7,060,066), Temporomandibular Joint Fossa-Eminence Prosthesis (patent no. 8,211,180), and Doppler Ultrasound for Identifying Material Properties of a Carpal Tunnel Anatomy (patent no. 8,216,148). The other authors have nothing to disclose.

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Clinical implications of basic researchUltrasound Elastography: The New Frontier in Direct Measurement of Muscle Stiffness

Abstract

Section snippets

Ultrasound elastography principles and techniques

Ultrasound elastography and muscle

Future directions

Conclusions

Arch Phys Med Rehabil

Arch Phys Med Rehabil

Clin Biomech (Bristol, Avon)

Ultrason Imaging

Spine J

Ultrasound Med Biol

Ultrasound Med Biol

Ultrasound Med Biol

Ultrasound Med Biol

Acad Radiol

Med Image Anal

Ultrasound Med Biol

J Biomech

J Mech Behav Biomed Mater

Ultrasound Med Biol

J Biomech

J Biomech

J Biomech

PM R

Magnetic resonance elastography: a review

Clin Anat

EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: basic principles and technology

Ultraschall Med

EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: clinical applications

Ultraschall Med

Ultrasound elastography for musculoskeletal applications

Br J Radiol

Selected methods for imaging elastic properties of biological tissues

Annu Rev Biomed Eng

AAPM/RSNA physics tutorial for residents: topics in US: beyond the basics: elasticity imaging with US

Radiographics

An overview of elastography: an emerging branch of medical imaging

Curr Med Imaging Rev

Muscle hardness measurement by using ultrasound elastography: a feasibility study

Acta Radiol

Office-based elastographic technique for quantifying mechanical properties of skeletal muscle

J Ultrasound Med

Diagnostic value of real-time sonoelastography in congenital muscular torticollis

J Ultrasound Med

Sonoelastography contribution in cerebral palsy spasticity treatment assessment, preliminary report: a systematic review of the literature apropos of seven patients

Med Ultrason

The change of intrinsic stiffness in gastrocnemius after intensive rehabilitation with botulinum toxin a injection in spastic diplegic cerebral palsy

Ann Rehabil Med

Propagation of spontaneously actuated pulsive vibration in human heart wall and in vivo viscoelasticity estimation

IEEE Trans Ultrason Ferroelectr Freq Control

Clinical implications of basic research
Ultrasound Elastography: The New Frontier in Direct Measurement of Muscle Stiffness