A validated model of passive skeletal muscle to predict force and intramuscular pressure

Wheatley, Benjamin B.; Odegard, Gregory M.; Kaufman, Kenton R.; Donahue, Tammy L. Haut

doi:10.1007/s10237-016-0869-z

Cited by 22 publications

(24 citation statements)

References 74 publications

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“…During both active contraction and passive deformation of muscle, intramuscular fluid pressures develop that can be measured empirically (e.g., ref. 1) and predicted computationally (2,3). These pressures typically fall within a range of 15 to 250 mmHg (4-6); however, much larger pressures of over 500 mmHg (7) and over 1,000 mmHg (8) have been reported.…”

mentioning

confidence: 97%

Internal fluid pressure influences muscle contractile force

Sleboda

Roberts

2019

Proc. Natl. Acad. Sci. U.S.A.

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Fluid fills intracellular, extracellular, and capillary spaces within muscle. During normal physiological activity, intramuscular fluid pressures develop as muscle exerts a portion of its developed force internally. These pressures, typically ranging between 10 and 250 mmHg, are rarely considered in mechanical models of muscle but have the potential to affect performance by influencing force and work produced during contraction. Here, we test a model of muscle structure in which intramuscular pressure directly influences contractile force. Using a pneumatic cuff, we pressurize muscle midcontraction at 260 mmHg and report the effect on isometric force. Pressurization reduced isometric force at short muscle lengths (e.g., −11.87% of P0 at 0.9 L0), increased force at long lengths (e.g., +3.08% of P0 at 1.25 L0), but had no effect at intermediate muscle lengths ∼1.1–1.15 L0. This variable response to pressurization was qualitatively mimicked by simple physical models of muscle morphology that displayed negative, positive, or neutral responses to pressurization depending on the orientation of reinforcing fibers representing extracellular matrix collagen. These findings show that pressurization can have immediate, significant effects on muscle contractile force and suggest that forces transmitted to the extracellular matrix via pressurized fluid may be important, but largely unacknowledged, determinants of muscle performance in vivo.

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confidence: 97%

Internal fluid pressure influences muscle contractile force

Sleboda

Roberts

2019

Proc. Natl. Acad. Sci. U.S.A.

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“…While each of these studies present advantages for modeling the passive response of skeletal muscle, we have chosen to use a similar approach to Yousefi et al (2018) with the extension of the model to include ECM collagen dispersion and muscle fiber stiffness. After applying assumptions for the low-stiffness isotropic ground matrix (Wheatley et al, 2017a) and nearincompressibility (Takaza et al, 2012), this model required five parameters to describe the hyperelastic response -two for the muscle fibers (stiffness and non-linearity) and three for the ECM (stiffness, direction, and dispersion). The advantage of this approach is a relatively low number of parameters while still enabling model robustness.…”

Section: Constitutive Modeling Of Experimental Datamentioning

confidence: 99%

Investigating Passive Muscle Mechanics With Biaxial Stretch

Wheatley

2020

Front. Physiol.

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Introduction: The passive stiffness of skeletal muscle can drastically affect muscle function in vivo, such as the case for fibrotic tissue or patients with cerebral palsy. The two constituents of skeletal muscle that dominate passive stiffness are the intracellular protein titin and the collagenous extracellular matrix (ECM). However, efforts to correlate stiffness and measurements of specific muscle constituents have been mixed, and thus the complete mechanisms for changes to muscle stiffness remain unknown. We hypothesize that biaxial stretch can provide an improved approach to evaluating passive muscle stiffness. Methods: We performed planar biaxial materials testing of passively stretched skeletal muscle and identified three previously published datasets of uniaxial materials testing. We developed and employed a constitutive model of passive skeletal muscle that includes aligned muscle fibers and dispersed ECM collagen fibers with a bimodal von Mises distribution. Parametric modeling studies and fits to experimental data (both biaxial and previously published) were completed. Results: Biaxial data exhibited differences in time dependent behavior based on orientation (p < 0.0001), suggesting different mechanisms supporting load in the direction of muscle fibers (longitudinal) and in the perpendicular (transverse) directions. Model parametric studies and fits to experimental data exhibited the robustness of the model (<20% error) and how differences in tissue stiffness may not be observed in uniaxial longitudinal stretch, but are apparent in biaxial stretch. Conclusion: This work presents novel materials testing data of passively stretched skeletal muscle and use of constitutive modeling and finite element analysis to explore the interaction between stiffness, constituent variability, and applied deformation in passive skeletal muscle. The results highlight the importance of biaxial stretch in evaluating muscle stiffness and in further considering the role of ECM collagen in modulating passive muscle stiffness.

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“…Recently, Grasa et al (2016) have introduced the CFs in their passive muscle model that can describe such an amazing stress-stretch behavior, but this model does not include the 3-D distribution of the CFs. Moreover, Wheatley et al (2017) have proposed a model for muscles in which it is possible to predict that the stiffest direction can be perpendicular to the MFs direction. But their model uses a lot of material parameters and cannot explain the cases in which the stiffest direction is neither parallel to the MFs direction nor perpendicular to them (Mohammadkhah et al 2016).…”

Section: A New Passive Muscle Modelmentioning

confidence: 99%

“…In these models, the existence of any reinforced direction other than the MF direction may impose some negative values on the anisotropic part of the stress tensor, which violates the convexity condition of the Strain Energy Function (SEF). To the authors knowledge, only for the cases in which the stiffest direction is perpendicular to the MF direction, the convexity condition is satisfied and it is possible to explain this behavior either using the invariants and structural tensors proposed by Schröder and Neff (2003) or assuming an ellipsoidal distribution of fibers in muscles in which the shortest diameter is along the direction of MFs (Wheatley et al 2017). So, it seems that the effects of the MF and CFs and their respective directions have to be separately defined in the passive CLs of muscle tissue.…”

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confidence: 99%

A new model of passive muscle tissue integrating Collagen Fibers: Consequences for muscle behavior analysis

Yousefi¹,

Nazari²,

Perrier³

et al. 2018

Journal of the Mechanical Behavior of Biomedical Materials

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Mechanical properties of muscle tissue are crucial in biomechanical modeling of the human body. Muscle tissue is a combination of Muscle Fibers (MFs) and connective tissue including collagen and elastin fibers. There are a lot of passive muscle models in the literature but most of them do not consider any distinction between Collagen Fibers (CFs) and MFs, or at least do not consider the mechanical effects of the CFs on the Three-Dimensional (3-D) behavior of tissue. As a consequence, unfortunately, they cannot describe the observed stress-stretch behavior in tissue in which the reinforced direction is not parallel to the MF direction. In this research, a new passive muscle model is presented, in which the CFs are separately considered in the formulation: they are distributed along the MFs in a cross-shaped arrangement. Thanks to this new architecture, a mechanical reinforced direction can be proposed, in addition to the muscle main fiber direction. The passive biomechanical properties of the genioglossus muscle of a bovine tongue have been measured under uniaxial tensile tests. To characterize the 3-D response of the tissue, tests have been performed in different directions with respect to the MF direction. Moreover, a Constitutive Law (CL) has been proposed for modeling this behavior. In addition to our measurements on the bovine genioglossus muscle, results published in the literature on experimental data from the longissimus dorsi of pigs and the chicken pectoralis muscle were used to appraise the applicability of the proposed model. It is demonstrated that the proposed passive muscle model provides an accurate description of the fiber-oriented nature of muscle tissue. Also, it has been shown that using Finite Element Analysis (FEA) it might be possible to predict the angle θ between CFs and MF.

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A validated model of passive skeletal muscle to predict force and intramuscular pressure

Cited by 22 publications

References 74 publications

Internal fluid pressure influences muscle contractile force

Internal fluid pressure influences muscle contractile force

Investigating Passive Muscle Mechanics With Biaxial Stretch

A new model of passive muscle tissue integrating Collagen Fibers: Consequences for muscle behavior analysis

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