Biomechanics Modeling of the Musculoskeletal Apparatus: Status and Key Issues

The aim of this review paper is to report on the current state of the art in creating in silico humans able to simulate the biomechanics of the human body at all scales of interest. The focus is on the musculoskeletal apparatus, although much of what is written is valid also for the biomechanical modeling of other organs. The state of the art of computational biomechanics at body, organ, tissue, and cell levels is briefly described and the most recent achievements in the area of multiscale models are discussed. In conclusion, the challenges to be faced to realize a true living human model are summarized. It is evident that the demands associated with some of these challenges greatly exceed the potential currently possessed by the computational biomechanics research community. Thus, to tackle them it will be necessary not only to coordinate all efforts in a coherent way,but also to mobilize much greater financial and human resources than are currently available.

[1]  M R Drost,et al.  Finite element modelling of contracting skeletal muscle. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[2]  A. Yettram,et al.  Stress and strain distribution within the intact femur: compression or bending? , 1996, Medical engineering & physics.

[3]  R Huiskes,et al.  From structure to process, from organ to cell: recent developments of FE-analysis in orthopaedic biomechanics. , 1993, Journal of biomechanical engineering.

[4]  Marcus G. Pandy,et al.  Dynamic Simulation of Human Movement Using Large-Scale Models of the Body , 2000, Phonetica.

[5]  Greg Turk,et al.  Texture synthesis on surfaces , 2001, SIGGRAPH.

[6]  D J Pearsall,et al.  The geometry of the psoas muscle as determined by magnetic resonance imaging. , 1994, Archives of physical medicine and rehabilitation.

[7]  Victor Sholukha,et al.  In vivo registration of both electrogoniometry and medical imaging: development and application on the ankle joint complex , 2006, IEEE Transactions on Biomedical Engineering.

[8]  W. Hayes,et al.  The compressive behavior of bone as a two-phase porous structure. , 1977, The Journal of bone and joint surgery. American volume.

[9]  S. Delp,et al.  Evaluation of a Deformable Musculoskeletal Model for Estimating Muscle–Tendon Lengths During Crouch Gait , 2001, Annals of Biomedical Engineering.

[10]  A Laib,et al.  A micro-computed tomography study of the trabecular bone structure in the femoral head. , 2003, Journal of musculoskeletal & neuronal interactions.

[11]  Marco Viceconti,et al.  An improved method for the automatic mapping of computed tomography numbers onto finite element models. , 2004, Medical engineering & physics.

[12]  E C Teo,et al.  Poroelastic Analysis of Lumbar Spinal Stability in Combined Compression and Anterior Shear , 2004, Journal of spinal disorders & techniques.

[13]  A Rohlmann,et al.  Hip Joint Forces During Load Carrying , 1997, Clinical orthopaedics and related research.

[14]  Guigen Zhang,et al.  Avoiding the material nonlinearity in an external fixation device. , 2004, Clinical biomechanics.

[15]  Y. Fung,et al.  Classical and Computational Solid Mechanics , 2001 .

[16]  Ray Vanderby,et al.  Application of a probabilistic microstructural model to determine reference length and toe-to-linear region transition in fibrous connective tissue. , 2003, Journal of biomechanical engineering.

[17]  Ming Zhang,et al.  Biomechanical responses of the intervertebral joints to static and vibrational loading: a finite element study. , 2003, Clinical biomechanics.

[18]  Kai-Nan An,et al.  Effects of plantar fascia stiffness on the biomechanical responses of the ankle-foot complex. , 2004, Clinical biomechanics.

[19]  P. B. Warren,et al.  Multiscale modelling of human hair , 2004, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[20]  Marco Viceconti,et al.  Primary stability of an anatomical cementless hip stem: a statistical analysis. , 2006, Journal of biomechanics.

[21]  Y Payan,et al.  The mesh-matching algorithm: an automatic 3D mesh generator for finite element structures. , 2000, Journal of biomechanics.

[22]  M. Krokos,et al.  Patient-specific muscle models for surgical planning , 2005, Third International Conference on Medical Information Visualisation--BioMedical Visualisation.

[23]  A. Kuo,et al.  A biomechanical analysis of muscle strength as a limiting factor in standing posture. , 1992, Journal of biomechanics.

[24]  Sheldon Weinbaum,et al.  Mechanotransduction and strain amplification in osteocyte cell processes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[25]  E. Schneider,et al.  Estimation of mechanical properties of cortical bone by computed tomography , 1991, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[26]  J M Crolet,et al.  Compact bone: numerical simulation of mechanical characteristics. , 1993, Journal of biomechanics.

[27]  Dwight G Nishimura,et al.  Real‐time imaging of skeletal muscle velocity , 2003, Journal of magnetic resonance imaging : JMRI.

[28]  L Blankevoort,et al.  A global verification study of a quasi-static knee model with multi-bundle ligaments. , 1996, Journal of biomechanics.

[29]  P. de Leva.  Adjustments to Zatsiorsky-Seluyanov's segment inertia parameters. , 1996, Journal of biomechanics.

[30]  M. Viceconti,et al.  Mechanical strength of a femoral reconstruction in paediatric oncology: A finite element study , 2003, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[31]  R. Crowninshield,et al.  A physiologically based criterion of muscle force prediction in locomotion. , 1981, Journal of biomechanics.

[32]  S. Jan.  Introducing Anatomical and Physiological Accuracy in Computerized Anthropometry for Increasing the Clinical Usefulness of Modeling Systems , 2005 .

[33]  P J Hunter,et al.  An anatomically based patient-specific finite element model of patella articulation: towards a diagnostic tool , 2005, Biomechanics and modeling in mechanobiology.

[34]  L J van Ruijven,et al.  The accuracy of joint surface models constructed from data obtained with an electromagnetic tracking device. , 2000, Journal of biomechanics.

[35]  E. Schneider,et al.  Influence of muscle forces on femoral strain distribution. , 1998, Journal of biomechanics.

[36]  Jenneke Klein-Nulend,et al.  A comparison of strain and fluid shear stress in stimulating bone cell responses—a computational and experimental study , 2005, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[37]  P. Tikuisis,et al.  Human body surface area: measurement and prediction using three dimensional body scans , 2001, European Journal of Applied Physiology.

[38]  Serge Van Sint Jan,et al.  Identifying the location of human skeletal landmarks: why standardized definitions are necessary--a proposal. , 2005, Clinical Biomechanics.

[39]  R. Keunings.  FINITE ELEMENT METHODS FOR INTEGRAL VISCOELASTIC FLUIDS , 2003 .

[40]  John J Callaghan,et al.  Kinematics, kinetics, and finite element analysis of commonplace maneuvers at risk for total hip dislocation. , 2003, Journal of biomechanics.

[41]  S. Delp,et al.  Accuracy of muscle moment arms estimated from MRI-based musculoskeletal models of the lower extremity. , 2000, Computer aided surgery : official journal of the International Society for Computer Aided Surgery.

[42]  Angelo Cappello,et al.  Automatic generation of accurate subject-specific bone finite element models to be used in clinical studies. , 2004, Journal of biomechanics.

[43]  R L Huston,et al.  On the dynamics of a human body model. , 1971, Journal of biomechanics.

[44]  W C Hayes,et al.  Mechanical properties of metaphyseal bone in the proximal femur. , 1991, Journal of biomechanics.

[45]  T. Keaveny,et al.  Dependence of yield strain of human trabecular bone on anatomic site. , 2001, Journal of biomechanics.

[46]  J. Laidlaw,et al.  ANATOMY OF THE HUMAN BODY , 1967, The Ulster Medical Journal.

[47]  Serge Van Sint Jan.  The VAKHUM project: virtual animation of the kinematics of the human , 2000 .

[48]  R Hutter,et al.  Mechanical modeling of soft biological tissues for application in virtual reality based laparoscopy simulators. , 2000, Technology and health care : official journal of the European Society for Engineering and Medicine.

[49]  M G Pandy,et al.  Computer modeling and simulation of human movement. , 2001, Annual review of biomedical engineering.

[50]  Klaus Bohndorf,et al.  Muscle cross-section measurement by magnetic resonance imaging , 2004, European Journal of Applied Physiology and Occupational Physiology.

[51]  A Gollhofer,et al.  Modelling, simulation and optimisation of a human vertical jump. , 1999, Journal of biomechanics.

[52]  M. O. Hellera,et al.  Musculo-skeletal loading conditions at the hip during walking and stair climbing , 2001 .

[53]  M. Pandy,et al.  Dynamic optimization of human walking. , 2001, Journal of biomechanical engineering.

[54]  J M T Penrose,et al.  Development of An Accurate Three-dimensional Finite Element Knee Model , 2002, Computer methods in biomechanics and biomedical engineering.

[55]  P. Rüegsegger,et al.  Morphometric analysis of human bone biopsies: a quantitative structural comparison of histological sections and micro-computed tomography. , 1998, Bone.

[56]  S. Delp,et al.  Cine phase-contrast magnetic resonance imaging as a tool for quantification of skeletal muscle motion. , 2003, Seminars in musculoskeletal radiology.

[57]  G. Bergmann,et al.  Hip contact forces and gait patterns from routine activities. , 2001, Journal of biomechanics.

[58]  W C Hayes,et al.  Finite element modeling of damage accumulation in trabecular bone under cyclic loading. , 1994, Journal of biomechanics.

[59]  E. Chao,et al.  Three-dimensional dynamic hip contact area and pressure distribution during activities of daily living. , 2006, Journal of biomechanics.

[60]  J Middleton,et al.  A stress analysis of the periodontal ligament under various orthodontic loadings. , 1991, European journal of orthodontics.

[61]  F.E. Zajac,et al.  An interactive graphics-based model of the lower extremity to study orthopaedic surgical procedures , 1990, IEEE Transactions on Biomedical Engineering.

[62]  B Agoram,et al.  Coupled macroscopic and microscopic scale modeling of fibrillar tissues and tissue equivalents. , 2001, Journal of biomechanical engineering.

[63]  J Bruns,et al.  Pressure distribution in the knee joint. Influence of flexion with and without ligament dissection. , 1994, Archives of orthopaedic and trauma surgery.

[64]  S. Majumdar,et al.  Processing and Analysis of In Vivo High-Resolution MR Images of Trabecular Bone for Longitudinal Studies: Reproducibility of Structural Measures and Micro-Finite Element Analysis Derived Mechanical Properties , 2002, Osteoporosis International.

[65]  Rik Huiskes,et al.  Effects of mechanical forces on maintenance and adaptation of form in trabecular bone , 2000, Nature.

[66]  B Melsen,et al.  Determination of stress levels and profiles in the periodontal ligament by means of an improved three-dimensional finite element model for various types of orthodontic and natural force systems. , 1991, Journal of biomedical engineering.

[67]  M G Pandy,et al.  A numerical method for simulating the dynamics of human walking. , 1988, Journal of biomechanics.

[68]  Victor Sholukha,et al.  Double-step registration of in vivo stereophotogrammetry with both in vitro 6-DOFs electrogoniometry and CT medical imaging. , 2006, Journal of biomechanics.

[69]  F. Zajac,et al.  Muscle coordination of maximum-speed pedaling. , 1997, Journal of biomechanics.

[70]  J. O'Connor,et al.  Strain distribution within the human femur due to physiological and simplified loading: Finite element analysis using the muscle standardized femur model , 2003, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[71]  M. Pandy.  Simple and complex models for studying muscle function in walking. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[72]  F Eckstein,et al.  Quantitative determination of articular pressure in the human shoulder joint. , 2000, Journal of shoulder and elbow surgery.

[73]  T. Keaveny,et al.  Trabecular bone modulus-density relationships depend on anatomic site. , 2003, Journal of biomechanics.

[74]  E Y Chao,et al.  A survey of finite element analysis in orthopedic biomechanics: the first decade. , 1983, Journal of biomechanics.

[75]  F E Zajac,et al.  Human standing posture: multi-joint movement strategies based on biomechanical constraints. , 1993, Progress in brain research.

[76]  W S Levine,et al.  An optimal control model for maximum-height human jumping. , 1990, Journal of biomechanics.

[77]  Stephen H. M. Brown,et al.  Less is more: high pass filtering, to remove up to 99% of the surface EMG signal power, improves EMG-based biceps brachii muscle force estimates. , 2004, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[78]  M. Dobelis,et al.  A Transversely Isotropic Hyperelastic Constitutive Model of the PDL. Analytical and Computational Aspects , 2003, Computer methods in biomechanics and biomedical engineering.

[79]  P. Huijing.  Muscular Force Transmission Necessitates a Multilevel Integrative Approach to the Analysis of Function of Skeletal Muscle , 2003, Exercise and sport sciences reviews.

[80]  B. van Rietbergen.  Micro-FE analyses of bone: state of the art. , 2001, Advances in experimental medicine and biology.

[81]  S. Majumdar,et al.  Quantification of Trabecular Bone Structure Using Magnetic Resonance Imaging at 3 Tesla—Calibration Studies Using Microcomputed Tomography as a Standard of Reference , 2005, Calcified Tissue International.

[82]  M G Pandy,et al.  Static and dynamic optimization solutions for gait are practically equivalent. , 2001, Journal of biomechanics.

[83]  David Taylor,et al.  Stress intensity variations in bone microcracks during the repair process. , 2004, Journal of theoretical biology.

[84]  A Seireg,et al.  A mathematical model for evaluation of forces in lower extremeties of the musculo-skeletal system. , 1973, Journal of biomechanics.

[85]  Marco Viceconti,et al.  A generalized procedure for predicting bone mass regulation by mechanical strain , 1990, Calcified Tissue International.

[86]  M G Pandy,et al.  Musculoskeletal Model of the Upper Limb Based on the Visible Human Male Dataset , 2001, Computer methods in biomechanics and biomedical engineering.

[87]  W A Kalender,et al.  A phantom for standardization and quality control in spinal bone mineral measurements by QCT and DXA: design considerations and specifications. , 1992, Medical physics.

[88]  E Y Chao,et al.  Internal forces and moments in the femur during walking. , 1997, Journal of biomechanics.

[89]  Peter A Huijing,et al.  The relative position of EDL muscle affects the length of sarcomeres within muscle fibers: experimental results and finite-element modeling. , 2003, Journal of biomechanical engineering.

[90]  Rik Huiskes,et al.  Erratum to “Stresses in the local collagen network of articular cartilage: a poroviscoelastic fibril-reinforced finite element study” [Journal of Biomechanics 37 (2004) 357–366] and “A fibril-reinforced poroviscoelastic swelling model for articular cartilage” [Journal of Biomechanics 38 (2005) 1195– , 2005 .

[91]  W R Walsh,et al.  A novel method for measuring medial compartment pressures within the knee joint in-vivo. , 2003, Journal of biomechanics.

[92]  S L Woo,et al.  A single integral finite strain viscoelastic model of ligaments and tendons. , 1996, Journal of biomechanical engineering.

[93]  Ronald Fedkiw,et al.  Creating and simulating skeletal muscle from the visible human data set , 2005, IEEE Transactions on Visualization and Computer Graphics.

[94]  Christian Hellmich,et al.  Can the diverse elastic properties of trabecular and cortical bone be attributed to only a few tissue-independent phase properties and their interactions? , 2004, Biomechanics and modeling in mechanobiology.

[95]  Angelo Cappello,et al.  Quantification of soft tissue artefact in motion analysis by combining 3D fluoroscopy and stereophotogrammetry: a study on two subjects. , 2005, Clinical biomechanics.

[96]  W. Hayes,et al.  The effect of impact direction on the structural capacity of the proximal femur during falls , 1996, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[97]  J H Keyak,et al.  Postfailure compressive behavior of tibial trabecular bone in three anatomic directions. , 1996, Journal of biomedical materials research.

[98]  Jason P. Halloran,et al.  Explicit finite element modeling of total knee replacement mechanics. , 2005, Journal of biomechanics.

[99]  J H Koolstra,et al.  Combined finite-element and rigid-body analysis of human jaw joint dynamics. , 2005, Journal of biomechanics.

[100]  R. Blickhan,et al.  A finite-element model for the mechanical analysis of skeletal muscles. , 2000, Journal of theoretical biology.

[101]  M. Pandy,et al.  Individual muscle contributions to support in normal walking. , 2003, Gait & posture.

[102]  Richard W. Bohannon,et al.  Association of physical performance measures with bone mineral density in postmenopausal women. , 2005, Archives of physical medicine and rehabilitation.

[103]  W. R. Jones,et al.  The deformation behavior and mechanical properties of chondrocytes in articular cartilage. , 1999, Osteoarthritis and cartilage.

[104]  J A Weiss,et al.  Computational modeling of ligament mechanics. , 2001, Critical reviews in biomedical engineering.

[105]  J. A. C. Martins,et al.  A numerical model of passive and active behavior of skeletal muscles , 1998 .

[106]  F. Zajac,et al.  Muscle force redistributes segmental power for body progression during walking. , 2004, Gait & posture.

[107]  Peter A Huijing,et al.  Effects of inter- and extramuscular myofascial force transmission on adjacent synergistic muscles: assessment by experiments and finite-element modeling. , 2003, Journal of biomechanics.

[108]  Marco Viceconti,et al.  Automatic generation of finite element meshes from computed tomography data. , 2003, Critical reviews in biomedical engineering.

[109]  R Huiskes,et al.  If bone is the answer, then what is the question? , 2000, Journal of anatomy.

[110]  T. Keller.  Predicting the compressive mechanical behavior of bone. , 1994, Journal of biomechanics.

[111]  W Baumann,et al.  The three-dimensional determination of internal loads in the lower extremity. , 1997, Journal of biomechanics.

[112]  S. Majumdar,et al.  In Vivo Assessment of Architecture and Micro-Finite Element Analysis Derived Indices of Mechanical Properties of Trabecular Bone in the Radius , 2002, Osteoporosis International.

[113]  R Huiskes,et al.  A theoretical framework for strain-related trabecular bone maintenance and adaptation. , 2005, Journal of biomechanics.

[114]  R. Huiskes,et al.  Hip-joint and abductor-muscle forces adequately represent in vivo loading of a cemented total hip reconstruction. , 2001, Journal of biomechanics.

[115]  Scott L Delp,et al.  Generating dynamic simulations of movement using computed muscle control. , 2003, Journal of biomechanics.

[116]  M. Biot.  Theory of Propagation of Elastic Waves in a Fluid‐Saturated Porous Solid. I. Low‐Frequency Range , 1956 .

[117]  M G Pandy,et al.  A parameter optimization approach for the optimal control of large-scale musculoskeletal systems. , 1992, Journal of biomechanical engineering.

[118]  Daniel M Espino,et al.  Stochastic Finite Element Analysis of Biological Systems: Comparison of a Simple Intervertebral Disc Model with Experimental Results , 2003, Computer methods in biomechanics and biomedical engineering.

[119]  M G Pandy,et al.  Optimal control of non-ballistic muscular movements: a constraint-based performance criterion for rising from a chair. , 1995, Journal of biomechanical engineering.

[120]  F Eckstein,et al.  In vivo contact areas of the knee in patients with patellar subluxation. , 2005, Journal of biomechanics.

[121]  C. E. Passerello,et al.  On human body dynamics , 1976, Annals of Biomedical Engineering.

[122]  R. Huiskes,et al.  A new method to determine trabecular bone elastic properties and loading using micromechanical finite-element models. , 1995, Journal of biomechanics.

[123]  A Ratcliffe,et al.  Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures. , 1992, Biomaterials.

[124]  M. Pandy,et al.  The Obstacle-Set Method for Representing Muscle Paths in Musculoskeletal Models , 2000, Computer methods in biomechanics and biomedical engineering.

[125]  B. Koopman,et al.  Three-dimensional finite element modeling of skeletal muscle using a two-domain approach: linked fiber-matrix mesh model. , 2001, Journal of biomechanics.

[126]  S L Woo,et al.  A validated three-dimensional computational model of a human knee joint. , 1999, Journal of biomechanical engineering.

[127]  F M van Krieken,et al.  A model of lower extremity muscular anatomy. , 1982, Journal of biomechanical engineering.

[128]  N. Kikuchi,et al.  A novel method for biomaterial scaffold internal architecture design to match bone elastic properties with desired porosity. , 2004, Journal of biomechanics.

[129]  Gordon Clapworthy,et al.  Volumetric texture synthesis for non-photorealistic volume rendering of medical data , 2005, The Visual Computer.

[130]  M. Zoghi,et al.  A Three-Dimensional Morphometrical Study of the Distal Human Femur , 1992, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[131]  W S Marras,et al.  A stochastic model of trunk muscle coactivation during trunk bending. , 1993, Spine.

[132]  David E Krebs,et al.  Corroboration of in vivo cartilage pressures with implications for synovial joint tribology and osteoarthritis causation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[133]  M. Ostoja-Starzewski,et al.  Modeling of bone at a single lamella level , 2004, Biomechanics and modeling in mechanobiology.

[134]  P M Cattaneo,et al.  A three-dimensional finite element model from computed tomography data: A semi-automated method , 2001, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[135]  N. Kikuchi,et al.  A homogenization sampling procedure for calculating trabecular bone effective stiffness and tissue level stress. , 1994, Journal of biomechanics.

[136]  Haiying Liu,et al.  Constructing Patient Specific Models for Correcting Intraoperative Brain Deformation , 2001, MICCAI.

[137]  Taiji Adachi,et al.  Changes in the Fabric and Compliance Tensors of Cancellous Bone due to Trabecular Surface Remodeling, Predicted by a Digital Image-based Model , 2004, Computer methods in biomechanics and biomedical engineering.

[138]  R Huiskes,et al.  On the modelling of long bones in structural analyses. , 1982, Journal of biomechanics.

[139]  F. Zajac.  Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. , 1989, Critical reviews in biomedical engineering.

[140]  S. Goldstein,et al.  The direct examination of three‐dimensional bone architecture in vitro by computed tomography , 1989, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.