Fibre and extracellular matrix contributions to passive forces in human skeletal muscles: An experimental based constitutive law for numerical modelling of the passive element in the classical Hill-type three element model

Abstract

The forces that allow body movement can be divided into active (generated by sarcomeric contractile proteins) and passive (sustained by intra-sarcomeric proteins, fibre cytoskeleton and extracellular matrix (ECM)). These are needed to transmit the active forces to the tendon and the skeleton. However, the relative contribution of the intra- and extra- sarcomeric components in transmitting the passive forces is still under debate. There is limited data in the literature about human muscle and so it is difficult to make predictions using multiscale models, imposing a purely phenomenological description for passive forces. In this paper, we apply a method for the experimental characterization of the passive properties of fibres and ECM to human biopsy and propose their clear separation in a Finite Element Model. Experimental data were collected on human single muscle fibres and bundles, taken from vastus lateralis muscle of elderly subjects. Both were progressively elongated to obtain two stress-strain curves which were fitted to exponential equations. The mechanical properties of the extracellular passive components in a bundle of fibres were deduced by the subtraction of the passive tension observed in single fibres from the passive tension observed in the bundle itself. Our results showed that modulus and tensile load bearing capability of ECM are higher than those of fibres and defined their quantitative characterization that can be used in macroscopic models to study their role in the transmission of forces in physiological and pathophysiological conditions.

Passive stiffness of fibrotic skeletal muscle in mdx mice relates to collagen architecture

“…The techniques used could also provide empirical data to expand the capacity of current computational models of muscle stiffness (Marcucci et al . 2019; Bleiler et al . 2019).…”

“…Critically, we also show that the alignment of these cables is significantly related to passive stiffness across genotypes and muscles, a general predictor of muscle stiffness. The techniques used could also provide empirical data to expand the capacity of current computational models of muscle stiffness (Marcucci et al 2019;Bleiler et al 2019). Collagen fibre alignment was indeed the most significant component of the ECM architecture-based model of muscle stiffness.…”

Extracellular matrix: an important regulator of cell functions and skeletal muscle development

“…Studies showed that the fiber network of ECM can be normalization and densification in the direction of force through stress-induced tension, which is conducive to muscle fiber contraction and cell migration [ 146 , 147 ]. Marcucci et al obtained the passive tension value of ECM fiber by subtracting the passive tension of muscle bundle and fiber, and then compared it with the passive tension of muscle fiber, proving that the modulus and tensile carrying capacity of ECM are higher than that of muscle fiber [ 148 ]. ECM hyperplasia can lead to the increase of stiffness and passive tension in skeletal muscles [ 149 ].…”

The Structure and Role of Intramuscular Connective Tissue in Muscle Function

“…As discussed below, that is now thought to be incorrect, and that their throughplane shear properties are more important. Using finite element models based upon the Hill-type three-element model, Marcucci et al (2019) have recently suggested that the contribution to the parallel elastic component in passive muscle elasticity may nevertheless be substantial.…”