Muscle as a collagen fiber reinforced composite:​ a review of force transmission in muscle and whole limb

Huijing, Peter A.

Affiliations

¹Instituut voor Fundamentele and Klinische Bewegingswetenschappen, Faculteit Bewegingswetenschappen, Vrije Universiteit, Amsterdam, Netherlands

²Integrated Biomedical Engineering for Restoration of Human Function, Biomedisch Technologisch Instituut, Universiteit Twente, Enschede, Netherland

Abstract

Even though no direct physiologic evidence proving that myo-tendinous junctions at the end of myofibers are sites of force transmission is available, these locations are accepted to support this function, because its specialized morphology resembles that of load-bearing membranes in structure and location: Its design is fit for force transmission of force exerted by myofibers to tendinous fibrous material. Shearing of the interface between these structures is thought to be stronger than direct tensile transmission. On the basis of morphological studies of ‘in-series fibered muscle’ and biomechanical modeling it has been argued previously that force could also be transmitted laterally from the tapered ends of myofibers onto in series myofiber via the intramuscular connective tissue component. Shearing of the interfaces between myofibers is hypothesized to be the mechanisms of transmission. The interfaces are made up of basal membranes of both myofibers and their common endomysium. The issue of lateral force transmission from myofibers has not been addressed for whole muscle, in which myofibers are attached at both ends to tendinous aponeuroses, nor is any direct experimental evidence available about possible functional importance of this phenomenon in whole muscle.

The primary objective of this presentation is to review available literature on myo-tendinous and myo-fascial force transmission, present evidence from experiments involving tenotomy, fasciatomy and aponeurotomy regarding its importance and consider implications for our thinking about muscle(s) and movement.

Links

DOI: 10.1016/S0021-9290(98)00186-9

PubMed: 10213024

WoS: 000079499500001

History

Received: 1998-11-17

Accepted: 1998-11-20

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Cited By (23)

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2002	Pappas GP, Asakawa DS, Delp SL, Zajac FE, Drace JE. Nonuniform shortening in the biceps brachii during elbow flexion. J Appl Physiol. June 2002;92(6):2381-2389.
2005	Blemker SS, Pinsky PM, Delp SL. A 3D model of muscle reveals the causes of nonuniform strains in the biceps brachii. J Biomech. April 1, 2005;38(4):657-665.
2023	Finni T, de Brito Fontana H, Maas H. Force transmission and interactions between synergistic muscles. J Biomech. May 2023;152:111575.
2023	Blemker SS. In vivo imaging of skeletal muscle form and function: 50 years of insight. J Biomech. September 2023;158:111745.
2005	Ng BH, Chou SM, Krishna V. The influence of gripping techniques on the tensile properties of tendons. Proc Inst Mech Eng Part H-J Eng Med. September 2005;219(5):349-354.
2017	Wheatley BB. Finite Element Analysis of Skeletal Muscle: A Validated Approach to Modeling Muscle Force and Intramuscular Pressure [PhD thesis]. Colorado State University; 2017.
2009	Wang I-N. Role of Heterotypic Cellular Interactions in the Regeneration of the Anterior Cruciate Ligament-to-Bone Interface [PhD thesis]. Columbia University; 2009.
2011	Bian W. Tissue Engineering of a Differentiated Skeletal Muscle Construct With Controllable Structure and Function [PhD thesis]. Duke University; 2011.
2015	Salimath AS. Biofunctional Hydrogels for Skeletal Muscle Constructs [PhD thesis]. Atlanta, GA: Georgia Institute of Technology; December 2015.
2021	Anderson SE. Aberrant Cellular Response and Muscle Regeneration Following Volumetric Muscle Loss [PhD thesis]. Atlanta, GA: Georgia Institute of Technology; August 2021.
2001	Pappas G. Characterization of Biceps Brachii Architecture and Contraction Mechanics Using Medical Imaging Techniques [PhD thesis]. Stanford University; February 2001.
2002	Asakawa DS. Magnetic Resonance Imaging of Skeletal Muscle Geometry and Motion After Surgery [PhD thesis]. Stanford University; October 2002.
2004	Blemker SS. 3D Modeling of Complex Muscle Architecture and Geometry [PhD thesis]. Stanford University; July 2004.
2011	Webb JD. Contributions of the Deltoid and Rotator Cuff to Shoulder Mobility and Stability: A 3D Finite Element Analysis [PhD thesis]. Stanford University; August 2011.
2010	Leonard TR. Force Production in Lengthened Myofibrils and Single Sarcomeres [PhD thesis]. Calgary, AB: University of Calgary; September 2010.
2020	Han S-w. Changes in Patellofemoral Joint Mechanics in the Presence of Quadriceps Muscle Imbalance [PhD thesis]. Calgary, AB: University of Calgary; August 2020.
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2002	Palmer ML. A Non-Linear Hierarchical Model of Stretch-Induced Injury to Skeletal Muscle Fibers [PhD thesis]. University of Michigan; 2002.
2014	Tan K. Characterising the Viscoelasticity of Soft Biological Tissues Under Large Deformation [PhD thesis]. University of New South Wales; March 2014.
2011	Sharafi B. Micromechanical Modeling of Skeletal Muscle: Insights Into Structure and Function At the Fiber and Fascicle Levels [PhD thesis]. Charlottesville, VA: University of Virginia; May 2011.
2018	Virgilio KM. Modeling Duchenne Muscular Dystrophy to Unravel the Complex Mechanisms of Disease Progression: From Biomechanics to Cell Physiology [PhD thesis]. Charlottesville, VA: University of Virginia; December 2018.
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