Exploration of trabecular bone nonlinear elasticity using time-of-flight modulation

Bone tissue contains microcracks that may affect its mechanical properties as well as the whole trabecular structure. The relationship between crack density and bone strength is nevertheless poorly understood. Linear ultrasound techniques being almost insensitive to the level of damage, we propose a method to measure acoustic nonlinearity in trabecular bone using time-of-flight modulation (TOFM) measurements. Ultrasonic short bursts times-of-flight (TOF) are modulated as a result of nonlinear interaction with a low-frequency (LF) wave in the medium. TOF variations are directly related to elastic modulus variations. Classical and nonclassical nonlinear parameters beta, delta, and alpha can be derived from these measurements. The method was validated in materials with classical, quadratic, nonlinear elasticity. In dense trabecular bone region, TOFM related to classical, quadratic, nonlinear elasticity as a function of the LF pressure exhibits tension-compression asymmetry. The TOFM amplitude measured in dense areas of trabecular bone is almost one order of magnitude higher than in a low-density area, but the linear parameters show much smaller variations: 5% for ultrasound propagation velocity and 100% for broadband ultrasonic attenuation (BUA). In high-density trabecular bone regions, beta depends on the LF pressure amplitude and can reach 400 at 50 kPa.