Quantifying changes in material properties of stroke-impaired muscle

Highlights

• Shear wave speed is faster in biceps brachii of paretic side of stroke survivor.

• Echo intensity is greater in biceps brachii of paretic side of stroke survivor.

• Muscle material properties and composition may be altered after stroke.

Abstract

Background

Material properties of muscles are clinically important parameters for evaluating altered muscle function. Stroke survivors display motor impairments almost immediately after the vascular event, and then gradually develop altered muscle properties. Little is known about the magnitude of these changes in muscle material properties, specifically stiffness. Previous measures of stiffness are limited to estimates of joint stiffness or groups of muscles. Thus, our aim was to determine changes in passive muscle stiffness and composition by measuring: (1) shear wave speed using shear wave ultrasound elastography and (2) echo intensity of the B-mode ultrasound images of the biceps brachii muscle in individuals who have had a stroke.

Methods

Shear wave ultrasound elastography and B-mode ultrasound images of the biceps brachii muscle of the paretic and non-paretic limbs of sixteen stroke survivors were captured at rest.

Findings

Our main results show that shear wave speed and echo intensity of the paretic side were on average 69.5% and 15.5% significantly greater than those of the non-paretic side, respectively. Differences in shear wave speed between the non-paretic and the paretic muscles were strongly correlated with differences in echo intensity, time since stroke, and with Fugl–Meyer scores.

Interpretation

Muscle stiffness and muscle composition, as indicated by SW speed and echo intensity, may be altered in stroke-impaired muscle at rest. These findings highlight the potential for SW elastography as a tool for both investigating the fundamental mechanisms behind changes in stroke-impaired muscle, and for evaluation of muscle mechanical properties as part of clinical examination.

Introduction

Stroke is one of the leading causes of long-term disability in the United States, with an annual incidence of approximately 800,000 persons (Lloyd-Jones et al., 2010). Stroke survivors routinely experience long-term motor and sensory impairments, especially in the upper extremity (Gray et al., 1990, Nakayama et al., 1994). These motor impairments include weakness for voluntary movement, spasticity, and impaired coordination, and they emerge almost immediately after the vascular event. Over time, material properties of muscles in the impaired limbs can also change gradually, further disrupting motor function, and adversely impacting the stroke survivor's quality of life. These material changes appear to be associated with the increasing accumulation of collagenous connective tissue (Lieber and Ward, 2013) and are accompanied by a progressive loss of skeletal muscle fibers (McLachlan and Chua, 1983, Tabary et al., 1972) and ultimately, with contractures, that potentially limit range of joint motion. Currently, the origins of these changes in material properties remain unclear. It is our objective in this study to compare material properties in spastic-paretic muscles with contralateral muscles of stroke survivors, using shear wave (SW) speed measurements as a surrogate measure of stiffness changes.

There have been a number of prior descriptions of muscle material properties in stroke survivors. Muscle stiffness has been shown to be different in individuals after a stroke (Katz and Rymer, 1989) in both lower (de Vlugt et al., 2010, Roy et al., 2011, Sinkjær and Magnussen, 1994) and upper extremity musculature (Chardon et al., 2010). However, these earlier stiffness estimates were made indirectly, such as by using kinematic protocols while recording muscle electrical activity, by calculating limb dynamics (Sinkjær and Magnussen, 1994), or by measuring the force generated during tendon indentation (Chardon et al., 2010).

Historically, the accurate quantification of passive muscle stiffness has only been possible through such approaches as cadaveric biomechanical studies, animal in situ experiments, muscle biopsies, and intra-operative force and torque measures. Obtaining non-invasive measurements that can quickly quantify changes in muscle stiffness of specific muscles in a clinical setting remains a challenge.

Recently, ultrasound imaging techniques appear to offer promising alternative approaches. Building upon traditional elastography (Brandenburg et al., 2014, Ophir et al., 1991), shear wave (SW) elastography, allows measurement of SW speed using either magnetic resonance imaging or ultrasound imaging, which is related to stiffness, specifically the shear modulus:

$$\mu =\rho V_s^2$$

where μ is the elastic shear modulus, ρ is the muscle mass density (ρ ≈ 1000 kg m^− 3), and V_s is the SW speed (Bercoff et al., 2004, Brandenburg et al., 2014, Muthupillai et al., 1995). The stiffer the tissue, the faster the SWs will travel. Here we use supersonic shear imaging (SSI) (Bercoff et al., 2004), a method that uses acoustic radiation forces to induce the SWs and subsequently measure the SW speed in muscle.

Several studies have investigated the stiffness of muscles using SSI in muscles of intact subjects, including the biceps brachii (Bouillard et al., 2012, Lacourpaille et al., 2012, Nordez and Hug, 2010, Yoshitake et al., 2014), gastrocnemius (Chernak et al., 2013, Lacourpaille et al., 2012, Maïsetti et al., 2012), and vastus lateralis muscles (Lacourpaille et al., 2012). SW speed has been reported to be higher in spastic muscles of children with cerebral palsy and in individuals with Duchenne muscular dystrophy compared to muscles of typically developing children (Kwon et al., 2012, Park and Kwon, 2012) and individuals without muscle disorders (Lacourpaille et al., 2015), respectively. By measuring the SW speed in muscle, we can indirectly estimate stiffness of muscle.

Accordingly, we sought to determine whether there are differences in SW speed in the biceps brachii muscles by comparing the paretic and contralateral limbs in stroke survivors. We also assessed the echogenicity of these muscles (measured as echo intensity from the B-mode image) and correlated our estimates of material properties with major clinical assessments, including the Fugl–Meyer scale (Gladstone et al., 2002), the modified Ashworth (Pandyan et al., 1999), and the modified Tardieu tests (Singh et al., 2011). (The Ashworth and Tardieu each provide a clinical measure of the severity of spasticity.) Conveniently, the quantification of muscle echo intensity from ultrasound images can also provide information about the tissue composition of muscle (Strasser et al., 2013) in that increased amounts of fibrous tissue can result in higher ultrasound echo intensity (Pillen et al., 2009a). Higher echo intensity has been associated with aging (Arts et al., 2010, Fukumoto et al., 2012, Strasser et al., 2013) and arise in children with myopathic and neuromuscular disorders (Lamminen et al., 1988, Pillen et al., 2007).