Elsevier

Journal of Biomechanics

Volume 44, Issue 3, 3 February 2011, Pages 424-429
Journal of Biomechanics

Ultrasound echo is related to stress and strain in tendon

https://doi.org/10.1016/j.jbiomech.2010.09.033Get rights and content

Abstract

The mechanical behavior of tendons has been well studied in vitro. A noninvasive method to acquire mechanical data would be highly beneficial. Elastography has been a promising method of gathering in vivo tissue mechanical behavior, but it has inherent limitations. This study presents acoustoelasticity as an alternative ultrasound-based method of measuring tendon stress and strain by reporting a relationship between ultrasonic echo intensity (B-mode ultrasound image brightness) and mechanical behavior of tendon in vitro. Porcine digital flexor tendons were cyclically loaded in a mechanical testing system while an ultrasonic echo response was recorded. We report that echo intensity closely follows the applied cyclic strain pattern in time with higher strain protocols resulting in larger echo intensity changes. We also report that echo intensity is related nonlinearly to stress and nearly linearly to strain. This indicates that ultrasonic echo intensity is related to the mechanical behavior in a loaded tissue by an acoustoelastic response, as previously described in homogeneous, nearly incompressible materials.

Acoustoelasticity is therefore able to relate strain-dependent stiffness and stress to the reflected echo, even in the processed B-mode signals reflected from viscoelastic and inhomogeneous material such as tendon, and is a promising metric to acquire in vivo mechanical data noninvasively.

Introduction

Tendons translate muscular contraction into skeletal movement, storing and releasing energy during motion (Ker et al., 1987). Understanding tendon mechanics is therefore essential to understand normal and pathologic movement and for analyzing the structural and mechanical consequence of injury. Thus far, tendon mechanical data have been obtained largely through in vitro experimentation (Abrahams, 1967, Cohen et al., 1976, Ker, 2007, Rigby et al., 1959, Woo et al., 1982). Though such studies provide essential basic mechanical information about the tissue, a noninvasive method to acquire mechanical data would allow patient-specific analysis and direct analysis of human pathologies that are poorly modeled by animals (e.g., rotator cuff). In vivo tendon loads have been computed using force plates or dynamometers and geometrical information (Maganaris and Paul, 1999, Maganaris and Paul, 2000, Riemersma et al., 1988) and/or with EMG studies of muscle (Lloyd and Besier, 2003). Direct studies of tendon are typically invasive and often rely on implanted strain gauges, providing only local measure of strain and a partial measure of mechanical behavior. EMG estimates contractile force in muscle (and thus in tendon), but it has a number of limiting factors such as cross talk from different muscles, passive tissue effects, different muscle lengths during contraction, and dynamic motion.

Recently, ultrasound imaging has been used to evaluate tissue strain and other mechanical properties (Samani et al., 2007, Skovorada et al., 1994, Skovorada et al., 1995). Many researchers have tried to evaluate tissue strain and mechanical properties using elastography, a technique originally proposed by Ophir et al. (1991), which maps strain distributions in tissues resulting from compression on the surface; since strain is inversely related to stiffness, elastography is an indirect method to estimate tissue stiffness (Doyley et al., 2000, Kallel et al., 1996, Kallel and Bertrand, 1996, Ponnekanti et al., 1992, Ponnekanti et al., 1995). Though researchers have used this technique to identify tissue properties, current elastographic methods have some inherent limitations.

Elastography tracks inhomogeneous echo reflections (“speckles” resulting from tissue heterogeneities) in ultrasound images during loading (usually using the transducer to apply compression); strain information calculated using distortions of these reflectors is related to mechanical properties via post hoc mechanical analysis. A limitation of elastography is that it is inherently linear, assuming that the material properties as well as ultrasound wave velocity do not change during strain measurement, which restricts analyses to small increments of compression. When soft tissues were tested under larger deformations and were therefore nonlinear in stiffness, significant errors occurred (Itoh et al., 2006, Zhi et al., 2007). This is problematic in soft tissues such as tendons as they are nonlinear in stiffness and undergo relatively large deformations during activity, reaching strains of several percent (elastography works best when strain increments are restricted to less than 1%). Another limitation is the commonly used method of compressive testing; tendon is loaded in tension in vivo, so interesting mechanical information is lost when only considering compressive transverse loads. These restrictions associated with standard elastographic methods limit its applicability to tendon. Finally, elastography measures strain. More data are needed, either stress or stiffness, to completely describe the mechanical behavior.

The theory of acoustoelasticity, developed byHughes and Kelly (1953) is based on the principle that the acoustic properties of a material are altered as the material is deformed and loaded, similar to a change in tension alters the pitch of a guitar string. Changes in acoustic properties caused by elastic deformation can be measured as a change in wave propagation velocity or reflected wave amplitude (Kobayashi and Vanderby, 2005, Kobayashi and Vanderby, 2007). Kobayashi and Vanderby, 2005, Kobayashi and Vanderby, 2007 derived the acoustoelastic relationship between reflected wave amplitude and mechanical behavior (strain-dependent stiffness and stress) in a deformed, nearly incompressible material using A-mode 1-D ultrasound. Despite signal processing, this phenomenon is also manifested in B-mode 2-D ultrasound, as the tensioning of tendon increases the intensity of the reflected ultrasonic echoes, leading to a brighter ultrasound image in B-mode. Examples of this acoustoelastic effect in soft tissues have been reported in the literature. For example, mean echogenicity has been correlated to the elastic modulus of the equine superficial digital flexor tendon (Crevier-Denoix et al., 2005), and softening of the human extensor tendons has been detected with sonoelastography (De Zordo et al., 2009). Pan et al. (1998) reported increasing echo intensity when skin underwent increase in strain (13–53%). The present study examines the relationship between ultrasonic echo intensity from standard clinical B-mode images and the stress–strain behavior of tendon during controlled loading in vitro. Its purpose is to examine whether this acoustoelastic phenomenon has the potential for the functional evaluation of tendon in vivo.

Section snippets

Specimen preparation

Eight porcine digital flexor tendons were carefully extracted from porcine legs (aged six months, sacrificed for an unrelated study) for ex vivo testing, leaving the bone and insertion site intact at the distal end. Bony ends were embedded in lightweight filler (Evercoat, Cincinnati, OH, USA) for ease of gripping. Specimens were kept hydrated in physiologic buffered saline (PBS) solution throughout preparation.

Mechanical testing

Mechanical testing was performed using a servohydraulic mechanical test system

Mechanical testing

When subjected to the cyclic loading protocol as shown in Fig. 2, the ultrasonic echo intensity of tendon was cyclic in behavior, and the echo intensity change increased with increase in strain level, shown in Fig. 3. This figure also shows a nonlinear dependence of peak echo intensity versus strain amplitude, and a deviation in the 6% strain curve from sinusoidal shape. Consequently, the relationship between echo intensity and strain is more nonlinear in this range than at lower strains. The

Discussion

In this study, cyclic loading experiments were carried out on excised porcine digital flexor tendons in a mechanical testing system. Cine ultrasound images were simultaneously recorded in B-mode in order to compare ultrasonic echo intensity changes (i.e., the average gray scale brightness in a selected region of interest in each image) to directly measured stress and strain. We show, for the first time, that an acoustoelastic effect known to exist in homogeneous materials can be easily observed

Conflict of interest statement

Two authors (RV and HK) hold a patent associated with some aspects of this concept for ultrasound analysis. No other authors have any conflicts of interest with the present study.

Acknowledgements

Support by the National Science Foundation (award 0553016) and National Institutes of Health (award R21 EB 008548) is gratefully acknowledged.

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