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TECHNICAL PAPERS: Soft Tissues

The Relative Position of EDL Muscle Affects the Length of Sarcomeres Within Muscle Fibers: Experimental Results and Finite-Element Modeling

[+] Author and Article Information
Huub Maas, Guus C. Baan

Instituut voor Fundamentele en Klinische Bewegingswetenschappen, Faculteit Bewegingswetenschappen, Vrije Universiteit, Van der Boechorststraat 9, 1081 BT, Amsterdam, The Netherlands

Peter A. Huijing

Instituut voor Fundamentele en Klinische Bewegingswetenschappen, Faculteit Bewegingswetenschappen, Vrije Universiteit, Van der Boechorststraat 9, 1081 BT, Amsterdam, The Netherlandsand Integrated Biomedical Engineering for Restoration of Human Function, Instituut voor Biomedische Technologie, Department of Biomechanical Engineering, Universiteit Twente, P.O. Box 217, 7500 AE Enschede, The Netherlands

Can A. Yucesoy, Bart H. F. J. M. Koopman, Henk J. Grootenboer

Integrated Biomedical Engineering for Restoration of Human Function, Instituut voor Biomedische Technologie, Department of Biomechanical Engineering, Universiteit Twente, P.O. Box 217, 7500 AE Enschede, The Netherlands

J Biomech Eng 125(5), 745-753 (Oct 09, 2003) (9 pages) doi:10.1115/1.1615619 History: Received February 03, 2003; Revised April 04, 2003; Online October 09, 2003
Copyright © 2003 by ASME
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References

Huijing,  P. A., and Baan,  G. C., 2001, “Extramuscular Myofascial Force Transmission Within the Rat Anterior Tibial Compartment: Proximo-Distal Differences in Muscle Force,” Acta Physiol. Scand., 173, pp. 297–311.
Maas,  H., Baan,  G. C., and Huijing,  P. A., 2001, “Intermuscular Interaction via Myofascial Force Transmission: Effects of Tibialis Anterior and Extensor Hallucis Longus Length on Force Transmission From Rat Extensor Digitorum Longus Muscle,” J. Biomech., 34, pp. 927–940.
Asakawa,  D. S., Blemker,  S. S., Gold,  G. E., and Delp,  S. L., 2002, “In Vivo Motion of the Rectus Femoris Muscle After Tendon Transfer Surgery,” J. Biomech., 35, pp. 1029–1037.
Maas, H., Baan, G. C., and Huijing, P. A., 2003, “Muscle Force Is Determined Also by Muscle-Relative Position: Isolated Effects,” J. Biomech. (in press).
Huijing,  P. A., and Baan,  G. C., 2003, “Myofascial Force Transmission: Muscle Relative Position and Length Co-Determine Agonist and Synergist Muscle Force,” J. Appl. Physiol., 94, pp. 1092–1107.
Huijing,  P. A., and Baan,  G. C., 2001, “Myofascial Force Transmission Causes Interaction Between Adjacent Muscles and Connective Tissue: Effects of Blunt Dissection and Compartmental Fasciotomy on Length Force Characteristics of Rat Extensor Digitorum Longus Muscle,” Arch. Physiol. Biochem., 109, pp. 97–109.
Berthier,  C., and Blaineau,  S., 1997, “Supramolecular Organization of the Subsarcolemmal Cytoskeleton of Adult Skeletal Muscle Fibers. A Review,” Biology of the Cell,89, pp. 413–434.
Patel,  T. J., and Lieber,  R. L., 1997, “Force Transmission in Skeletal Muscle: From Actomyosin to External Tendons,” Exercise Sport Sci. Rev., 25, pp. 321–363.
Yucesoy,  C., Koopman,  B., Huijing,  P., and Grootenboer,  H., 2002, “Three-Dimensional Finite-Element Modeling of Skeletal Muscle Using a Two-Domain Approach: Linked Fiber-Matrix Mesh Model,” J. Biomech., 35, pp. 1253–1262.
Yucesoy, C. A., Koopman, H. F. J. M., Huijing, P. A., and Grootenboer, H. J., 2001, “Finite-Element Modeling of Intermuscular Interactions and Myofascial Force Transmission,” Proceedings of 23rd Annual International Conference of the IEEE Engineering in Medicine and Biology Society.
Yucesoy, C. A., Koopman, B. H. F. J. M., Baan, G. C., Grootenboer, H. J., and Huijing, P. A., 2002, “Inter- and Extramuscular Myofascial Force Transmission Affect Muscular Mechanics Substantially: A Review of Recent Results,” Proceedings of the 9th Dutch Annual Conference on Biomedical Engineering, pp. 159–163.
Huijing,  P. A., Maas,  H., and Baan,  G. C., 2003, “Compartmental Fasciotomy and Isolating a Muscle From Neighboring Muscles Interfere With Myofascial Force Transmission Within the Rat Anterior Crural Compartment,” J. Morphol., 256, pp. 306–321.
Van der Linden, B. J. J. J., 1998, Mechanical Modeling of Skeletal Muscle Functioning, Department of Mechanical Engineering, University of Twente, Enschede.
Zuurbier,  C. J., Everard,  A. J., Van der Wees,  P., and Huijing,  P. A., 1994, “Length-Force Characteristics of the Aponeurosis in the Passive and Active Muscle Condition and in the Isolated Condition,” J. Biomech., 27, pp. 445–453.
Woo,  S. L., Ritter,  M. A., Amiel,  D., Sanders,  T. M., Gomez,  M. A., Kuei,  S. C., Garfin,  S. R., and Akeson,  W. H., 1980, “The Biomechanical and Biochemical Properties of Swine Tendons—Long Term Effects of Exercise on the Digital Extensors,” Connect. Tissue Res., 7, pp. 177–183.
Scott,  S. H., and Loeb,  G. E., 1995, “Mechanical Properties of Aponeurosis and Tendon of the Cat Soleus Muscle During Whole-Muscle Isometric Contractions,” J. Morphol., 224, pp. 73–86.
Ettema,  G. J. C., and Huijing,  P. A., 1989, “Properties of the Tendinous Structures and Series Elastic Component of Edl Muscle-Tendon Complex of the Rat,” J. Biomech., 22, pp. 1209–1215.
Kawakami,  Y., and Lieber,  R. L., 2000, “Interaction Between Series Compliance and Sarcomere Kinetics Determines Internal Sarcomere Shortening During Fixed-End Contraction,” J. Biomech., 33, pp. 1249–1255.
Banus,  M. G., and Zetlin,  A. M., 1938, “The Relation of Isometric Tension to Length in Skeletal Muscle,” J. Cell. Comp. Physiol., 12, pp. 403–420.
Strumpf,  R. K., Humphrey,  J. D., and Yin,  F. C., 1993, “Biaxial Mechanical Properties of Passive and Tetanized Canine Diaphragm,” Am. J. Physiol. 265, pp. H469–475.
Huijing,  P. A., 1999, “Muscle as a Collagen Fiber Reinforced Composite: A Review of Force Transmission in Muscle and Whole Limb,” J. Biomech., 32, pp. 329–345.
Maas, H., Yucesoy, C. A., Baan, G. C., and Huijing, P. A., 2003, “Implications of Muscle Relative Position as a Co-Determinant of Isometric Muscle Force: A Review and Some Experimental Results,” J. Mech. Med. Biol., 3 , pp. 145–168.
Huijing,  P. A., 1995, “Parameter Interdependence and Success of Skeletal Muscle Modelling,” Hum. Mov. Sci., 14, pp. 443–486.
Pollack,  G. H., Horowitz,  A., Wussling,  M., and Trombitas,  K., 1993, “Shortening-Induced Tension Enhancement: Implication for Length-Tension Relations,” Adv. Exp. Med. Biol., 332, pp. 679–688.
Granzier,  H. L., and Pollack,  G. H., 1990, “The Descending Limb of the Force-Sarcomere Length Relation of the Frog Revisited,” J. Physiol. (London), 421, pp. 595–615.
Ettema,  G. J. C., and Huijing,  P. A., 1994, “Effects of Distribution of Muscle Fiber Length on Active Length-Force Characteristics of Rat Gastrocnemius Medialis,” Anat. Rec., 239, pp. 414–420.
Willems,  M. E. T., and Huijing,  P. A., 1994, “Heterogeneity of Mean Sarcomere Length in Different Fibres: Effects on Length Range of Active Force Production in Rat Muscle,” Eur. J. Appl. Physiol., 68, pp. 489.
Fukunaga,  T., Ichinose,  Y., Ito,  M., Kawakami,  Y., and Fukashiro,  S., 1997, “Determination of Fascicle Length and Pennation in a Contracting Human Muscle in Vivo,” J. Appl. Physiol., 82, pp. 354–358.
Savelberg,  H. H., Willems,  P. J., Baan,  G. C., and Huijing,  P. A., 2001, “Deformation and Three-Dimensional Displacement of Fibers in Isometrically Contracting Rat Plantaris Muscles,” J. Morphol., 250, pp. 89–99.
Van Bavel,  H., Drost,  M. R., Wielders,  J. D. L., Huyghe,  J. M., Huson,  A., and Janssen,  J. D., 1996, “Strain Distribution on Rat Medial Gastrocnemius (Mg) During Passive Stretch,” J. Biomech., 29, pp. 1069–1074.
Pappas,  G. P., Asakawa,  D. S., Delp,  S. L., Zajac,  F. E., and Drace,  J. E., 2002, “Nonuniform Shortening in the Biceps Brachii During Elbow Flexion,” J. Appl. Physiol., 92, pp. 2381–2389.
Huijing,  P. A., Baan,  G. C., and Rebel,  G. T., 1998, “Non-Myotendinous Force Transmission in Rat Extensor Digitorum Longus Muscle,” J. Exp. Biol., 201, pp. 683–691.
Jaspers,  R. T., Brunner,  R., Pel,  J. J., and Huijing,  P. A., 1999, “Acute Effects of Intramuscular Aponeurotomy on Rat Gastrocnemius Medialis: Force Transmission, Muscle Force and Sarcomere Length,” J. Biomech., 32, pp. 71–79.
Street,  S. F., and Ramsey,  R. W., 1965, “Sarcolemma Transmitter of Active Tension in Frog Skeletal Muscle,” Science,149, pp. 1379–1380.
Street,  S. F., 1983, “Lateral Transmission of Tension in Frog Myofibres: A Myofibrillar Network and Transverse Cytoskeletal Connections are Possible Transmitters,” J. Cell Physiol., 114, pp. 346–364.
Goldberg,  S. J., Wilson,  K. E., and Shall,  M. S., 1997, “Summation of Extraocular Motor Unit Tensions in the Lateral Rectus Muscle of the Cat,” Muscle Nerve, 20, pp. 1229–1235.
Monti,  R. J., Roy,  R. R., Hodgson,  J. A., and Edgerton,  V. R., 1999, “Transmission of Forces Within Mammalian Skeletal Muscles,” J. Biomech., 32, pp. 371–380.
Monti,  R. J., Roy,  R. R., and Edgerton,  V. R., 2001, “Role of Motor Unit Structure in Defining Function,” Muscle Nerve, 24, pp. 848–866.
Jaspers,  R. T., Brunner,  R., Baan,  G. C., and Huijing,  P. A., 2002, “Acute Effects of Intramuscular Aponeurotomy and Tenotomy on Multitendoned Rat Edl: Indications for Local Adaptation of Intramuscular Connective Tissue,” Anat. Rec., 266, pp. 123–135.
Lieber,  R. L., Loren,  G. J., and Friden,  J., 1994, “In Vivo Measurement of Human Wrist Extensor Muscle Sarcomere Length Changes,” J. Neurophysiol., 71, pp. 874–881.
Lieber,  R. L., Ljung,  B. O., and Friden,  J., 1997, “Intraoperative Sarcomere Length Measurements Reveal Differential Design of Human Wrist Extensor Muscles,” J. Exp. Biol., 200, pp. 19–25.

Figures

Grahic Jump Location
The experimental setup and the muscle model. (a) Lateral view of the anterior crural compartment in the experimental set-up after TA and EHL muscles were almost fully removed. The intervention involved fasciotomy of the anterior crural compartment and excising TA and EHL muscles. A small piece of TA muscle was left attached to the compartment to prevent damage to the neurovascular tract of EDL muscle. A connective tissue sheet all along EDL muscle supporting its nerves and blood vessels was left intact. Thus all intermuscular myofascial pathways and a part of the extramuscular myofascial pathways were excluded. The footplate and the femur clamp are indicated. The smallest division of the ruler shown represents 0.5 mm. (b) A schematic view of the experimental set-up, seen from above. FT 1 indicates the force transducer connected to the distal tendons of EDL muscle, FT 2 indicates the force transducer connected to the proximal tendon of EDL. The force transducers were mounted on a single axis micropositioner. Each relative position of EDL muscle (Δ EDL muscle position) was obtained by repositioning FT 1 as well as FT 2, in a variable order, one mm in proximal direction. Δ EDL muscle position=0 refers to the most distal position of EDL muscle. The distance between FT 1 and FT 2, i.e. d(FT1-FT2) and, thus also the muscle-tendon complex length of EDL muscle (lm+t EDL) remained constant. (c) Geometry of the muscle model. The geometry is defined by the contour of a longitudinal slice of the rat EDL muscle belly. The muscle model is composed of three muscle elements in series, representing a fascicle, and six muscle elements in parallel. A 3-D local coordinate system is used for the analysis and presentation of the results. At the nodes indicated with a “+” sign the extramuscular connections are made and the ones marked also with a square are stiffer as they represent the connective tissues supporting the neurovascular tract of EDL muscle.
Grahic Jump Location
Experimentally measured as well as modeled forces of EDL muscle, kept at constant high length (i.e. lo+2 mm), with varying EDL muscle relative positions. (a) Experimentally measured proximal and distal total and passive forces of EDL muscle plotted as a function of EDL muscle relative position. (b) Experimental data and lfmm model data for total proximal and distal EDL muscle force normalized for maximal force (Fmax) plotted as a function of EDL muscle relative position. EDL muscle relative position is expressed as the deviation from the most distal position. The Fm, Fmp, and Fmax represent total, passive and maximal force, respectively. Note that in A different y-axes with different scaling factors are shown for total (left axis) and passive forces (right axis). Values are shown as mean±SE (n=6).
Grahic Jump Location
Fiber direction strains at different locations within the fiber mesh. Comparison of strains between elements arranged in series of EDL model kept at constant high length (i.e. lo+2 mm), for selected EDL muscle relative positions (i.e. Δ EDL muscle position=0, 7 and 9 mm). For four fascicle sections, the fiber direction strains are plotted as a function of fascicle number. Each fascicle is indicated by a number from 1 to 7 (lower panel). Differences of strain between sections arranged in series within a fascicle provide a measure of the distribution of lengths of sarcomeres arranged in series within muscle fibers. Strain is defined as the ratio of the change in length to the original length. Zero strain in the model is assumed to represent the undeformed state of sarcomeres (i.e., sarcomere length≅2.5 μm) in the passive condition, at initial muscle length (28.7 mm). Positive strain shows lengthening and negative strain shows shortening of the sarcomeres with respect to this undeformed state.
Grahic Jump Location
Fiber direction mean strains of different fascicles within the fiber mesh. Comparison of mean strains between fascicles of EDL model kept at high length (i.e., lo+2 mm), for selected EDL muscle relative positions (i.e., Δ EDL muscle position=0, 7 and 9 mm). Mean fiber direction strains are plotted as a function of fascicle number. Each fascicle is indicated by a number from 1 to 7 (lower panel). Mean fiber direction strain was calculated at nodes of the myofiber elements (in the fiber mesh) in series representing a fascicle. Mean fiber direction strain indicates the distribution of fiber mean sarcomere length in parallel among muscle fibers. Strain is defined as the ratio of the change in length to the original length. Zero strain in the model is assumed to represent the undeformed state of sarcomeres (i.e., sarcomere length≅2.5 μm) in the passive condition, at initial muscle length (28.7 mm). Positive strain shows lengthening and negative strain shows shortening of the sarcomeres with respect to this undeformed state.
Grahic Jump Location
Fiber direction stress within the fiber mesh of the EDL model kept at high length (i.e., lo+2 mm), for selected EDL muscle relative positions (i.e., Δ EDL muscle position=0, 7 and 9 mm). The dotted line contour indicates muscle geometry of isolated EDL model at the initial length. The fiber direction (arrow) as well as proximal and distal ends of the model are shown.

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