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And Extramuscular Myofascial Force Transmission INTRA-, INTER- AND EXTRAMUSCULAR MYOFASCIAL FORCE TRANSMISSION A COMBINED FINITE ELEMENT MODELING AND EXPERIMENTAL APPROACH Can. A. Yücesoy Graduation Committee: Chairman and Secretary: Prof. dr. C. Hoede Universiteit Twente Promotors: Prof. dr. P.A.J.B.M. Huijing Vrije Universiteit / Universiteit Twente Prof. dr. ir. H.J. Grootenboer Universiteit Twente Assistant Promotor: Dr. ir. H.F.J.M. Koopman Universiteit Twente Members: Prof. dr. A. de Boer Universiteit Twente Prof. dr. ir. P.H. Veltink Universiteit Twente Prof. dr. J.H. van Dieën Vrije Universiteit Prof. dr. F.C.T. van der Helm Technische Universiteit Delft / Universiteit Twente Dr. ir. J.M.R.J. Huyghe Technische Universiteit Delft / Universiteit Maastricht Cover design: Ecem Ecevit Pogge and Eda Ünlü Yücesoy ISBN: 90-365-1933-0 © C. A. Yücesoy, Enschede 2003 Printed by DPP-Utrecht B.V., Utrecht, The Netherlands INTRA-, INTER- AND EXTRAMUSCULAR MYOFASCIAL FORCE TRANSMISSION A COMBINED FINITE ELEMENT MODELING AND EXPERIMENTAL APPROACH PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Universiteit Twente, op gezag van de rector magnificus, prof. dr. F.A. van Vught, volgens besluit van het College voor Promoties in het openbaar te verdedigen op vrijdag 27 juni 2003 te 15:00 uur door Can Ali Yücesoy geboren op 13 juli 1970 te Ankara, Turkije. Promotors: Prof. dr. P.A.J.B.M. Huijing Prof. dr. ir. H.J. Grootenboer Assistant Promotor: Dr. ir. H.F.J.M. Koopman The following parts of this thesis have been published or submitted for publication Yucesoy, C. A., Koopman, H. J. F. M., Huijing, P. A. and Grootenboer, H. J., 2002. Three- dimensional finite element modeling of skeletal muscle using a two-domain approach: Linked fiber-matrix mesh model. Journal of Biomechanics 35, 1253-1262. Yucesoy, C. A., Koopman, H. J. F. M., Huijing, P. A. and Grootenboer, H. J., 2001. Finite element modeling of intermuscular interactions and myofascial force transmission. Proceedings of the 23rd Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Istanbul, Turkey. Yucesoy, C. A., Koopman, H. J. F. M., Guus, C. B., Grootenboer, H. J. and Huijing, P. A., 2003. Extramuscular myofascial force transmission: Experiments and finite element modeling. Archives of Physiology and Biochemistry, in revision. Yucesoy, C. A., Koopman, H. J. F. M., Guus, C. B., Grootenboer, H. J. and Huijing, P. A., 2003. Effects of inter- and extramuscular myofascial force transmission on adjacent synergistic muscles: Assessment by experiments and finite element modeling. Journal of Biomechanics, in press. Yucesoy, C. A., Maas, H., Koopman, H. J. F. M., Grootenboer, H. J. and Huijing, P. A., 2003. Finite element modeling of relative position of a muscle: Effects of extramuscular myofascial force transmission. International Journal of Mechanics in Medicine and Biology, in press. Contents Acknowledgements 9 Summary 11 Chapter 1 Introduction 15 Chapter 2 Three-dimensional finite element modeling of skeletal muscle 35 using a two-domain approach: Linked fiber-matrix mesh model Chapter 3 Finite element modeling of intermuscular interactions and 53 myofascial force transmission Chapter 4 Extramuscular myofascial force transmission: Experiments 63 and finite element modeling Chapter 5 Effects of inter- and extramuscular myofascial force 85 transmission on adjacent synergistic muscles: Assessment by experiments and finite element modeling Chapter 6 Finite element modeling of relative position of a muscle: 111 Effects of extramuscular myofascial force transmission Chapter 7 General discussion 133 Appendix A Large deformation analysis of solid continuum with 151 material and geometric nonlinearities Appendix B Implementation of the finite element method 161 Appendix C Anatomical and physiological terms 167 Acknowledgements This research was carried out at the Biomechanical Engineering research group of the Mechanical Engineering Department, Universiteit Twente, Enschede. The experimental studies were conducted at the Myology Laboratory of the Institute of Human Movement Sciences, Vrije Universiteit, Amsterdam. I would like to gratefully acknowledge these institutions. This work involves a multidiscipline study in which physiological questions were addressed employing principles of solid mechanics. Therefore, this thesis is a result of a wonderful teamwork and it would have never been completed otherwise. In the first place, I would like to express my gratitude to Peter Huijing for his excellent supervision, for making me affiliated with the physiological aspects of the research, and for helping me gain the skills of interpreting the results of mechanical analyses leading to physiological conclusions. His never-ending enthusiasm for the research was most inspiring and encouraging. I would also like to thank him very much for his support and concern in several situations, which made my experience in the Netherlands more pleasant and comfortable. Henk Grootenboer is “the” role model; a mechanical engineer doing research in the field of biomechanics would want to be. I am grateful for his exceptional supervision. I would like to thank my assistant promotor, Bart Koopman for the very valuable weekly discussions and for helping me resolve several issues. It was most pleasurable to work with him. Guus Baan, with his infinite energy, was the person who made the physiological experiments possible. I learned so much from him and had great long days working in the lab with him. Thanks very much Guus. Huub Maas, my inspiring colleague in Vrije Universiteit, Amsterdam. It was a real pleasure to cooperate with him. I feel honored to have worked with them. I would like to thank my colleagues Arthur, Arturo, Miguel, Hendrik-Jan, Bart, Herman, Edsko, Stella, Theo, Ray, Marian, Freek, Jan, Edwin, Ralf, Jasper, Yvonne, Nikolai, Johan, Willem, and Richard for their helps, ideas and support. Two of my colleagues, Laurens Kamman and Anton Sanders strongly deserve a distinguished acknowledgement. From helping me find my ways in the first days to supporting me as my paranimfen in the last day, they were a special part of my experience in the Netherlands. Special thanks to Murat, Tolga, Sinan, Ayse, and Atila for their everlasting support and friendship, 9 Tuna, Herman, and Gabriela for their inspiration and helps, Hüseyin, Belgin, Marieke, Karin, Caner, Evren, Sıtkı and Sonia for their supports and friendship in the Netherlands, Trudi van Rooijen for the great times in the Netherlands and in Turkey, and my former colleagues Alptekin, and Senih for their encouragement and for fruitful scientific discussions. I would like to express my gratitude for my parents who had done every sacrifice necessary to give me a good future. Finally, I would especially like to thank my wife Eda. Bızbızım tesekkürler. Can A. Yücesoy June, 2003 10 Summary Exertion of force onto the bony skeleton is the fundamental requirement for animals to move their limbs in order to accomplish several tasks. Muscle is the motor for generation of the necessary force. Yet, exertion of force involves not only generation of force but also transmission of it. Conceivably due to its highly specialized morphology, the myotendinous junction (the junction between the ends of muscle fibers and the aponeurosis) has been very widely accepted to be the exclusive site for transmission of force from muscle fibers where the force is generated. From this assumption, it follows that commonly individual skeletal muscles are considered as independent functional units having unique muscle length-force characteristics. However, muscle fibers and the extracellular matrix are connected not only at the myotendinous junctions, but also along the remainder of the full perimeter surface of the muscle fibers. Experiments have shown that these connections play a significant role in force transmission. Moreover, neighboring muscles are connected to each other as well as to the boundaries of the compartments within which they operate. This implicates that transmission of muscle force is not limited to the myotendinous junction exclusively, but it also involves a complex network of pathways provided by the myofascial apparatus. One of the goals of this study was to study, quantitatively, the importance of effects of myofascial force transmission on muscle length-force characteristics and on distributions of lengths of sarcomeres. In addition, the hypothesis was tested that, if force is transmitted between muscles as well as from muscles to nonmuscular structures via myofascial pathways, individual muscles should not be viewed as fully independent functional units. These hypotheses were tested using a combined finite element modeling and experimental approach. Both approaches include methods that were designed specifically to study myofascial force transmission. The model is equipped with two elastically linked meshes within the same space to represent the muscle fibers and its extracellular matrix. The experiments were performed with connective tissues intact as much as possible or manipulated for specific effects. As a first application, a model of isolated medial gastrocnemius muscle of the rat was used to study transmission of force between the muscle fibers and the extracellular matrix via the transsarcolemmal connections (Chapter 2). The stiffness of links at selected locations within the muscle was manipulated, i.e. certain links were made much more compliant than the highly stiff links at other locations within the modeled muscle. Note that such altered connections between
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