Modeling distraction osteogenesis: analysis of the distraction rate

Distraction osteogenesis is a useful technique aimed at inducing bone formation in widespread clinical applications. One of the most important factors that conditions the success of bone regeneration is the distraction rate. Since the mechanical environment around the osteotomy site is one of the main factors that affects both quantity and quality of the regenerated bone, we have focused on analyzing how the distraction rate influences on the mechanical conditions and tissue regeneration. Therefore, the aim of the present work is to explore the potential of a mathematical algorithm to simulate clinically observed distraction rate related phenomena that occur during distraction osteogenesis. Improvements have been performed on a previous model (Gómez-Benito et al. in J Theor Biol 235:105–119, 2005) in order to take into account the load history. The results obtained concur with experimental findings: a slow distraction rate results in premature bony union, whereas a fast rate results in a fibrous union. Tension forces in the interfragmentary gap tissue have also been estimated and successfully compared with experimental measurements.

[1]  Elizabeth G Loboa,et al.  Mechanobiology of mandibular distraction osteogenesis: Finite element analyses with a rat model , 2005, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[2]  A. Yokobori,et al.  The mechanical behavior and morphological structure of callus in experimental callotasis. , 1994, Bio-medical materials and engineering.

[3]  Dennis R. Carter,et al.  Mechanobiology of Skeletal Regeneration , 1998, Clinical orthopaedics and related research.

[4]  F. Pauwels,et al.  Eine neue Theorie ber den Einflu mechanischer Reize auf die Differenzierung der Sttzgewebe: Zehnter Beitrag zur funktionellen Anatomie und kausalen Morphologie des Sttzapparates , 1960 .

[5]  M J Gómez-Benito,et al.  Computational simulation of fracture healing: influence of interfragmentary movement on the callus growth. , 2007, Journal of biomechanics.

[6]  J. Aronson,et al.  Sustained proliferation accompanies distraction osteogenesis in the rat , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[7]  Stuart J Warden,et al.  Cellular accommodation and the response of bone to mechanical loading. , 2005, Journal of biomechanics.

[8]  V. A. Gibson,et al.  Model of flexural fatigue damage accumulation for cortical bone , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[9]  Birte Melsen,et al.  Three-Dimensional Finite Element Analysis of the Mandible and Temporomandibular Joint on Simulated Occlusal Forces before and after Vertical Ramus Elongation by Distraction Osteogenesis , 2005, The Journal of craniofacial surgery.

[10]  Antonio Boccaccio,et al.  Tissue differentiation and bone regeneration in an osteotomized and distracted mandible , 2006 .

[11]  I. Shapiro,et al.  Hypertrophic Chondrocytes , 1990, Annals of the New York Academy of Sciences.

[12]  Marjolein C H van der Meulen,et al.  Beneficial effects of moderate, early loading and adverse effects of delayed or excessive loading on bone healing. , 2003, Journal of biomechanics.

[13]  J. Dequeker,et al.  Distraction Bone Healing Versus Osteotomy Healing: A Comparative Biochemical Analysis , 1998, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[14]  G A Ilizarov,et al.  Clinical application of the tension-stress effect for limb lengthening. , 1990, Clinical orthopaedics and related research.

[15]  L. Claes,et al.  Magnitudes of local stress and strain along bony surfaces predict the course and type of fracture healing. , 1998, Journal of biomechanics.

[16]  G A Ilizarov,et al.  The tension-stress effect on the genesis and growth of tissues: Part II. The influence of the rate and frequency of distraction. , 1989, Clinical orthopaedics and related research.

[17]  G. Tajana,et al.  The structure and development of osteogenetic repair tissue according to Ilizarov Technique in man. Characterization of extracellular matrix. , 1989, Orthopedics.

[18]  Gavriil A. Ilizarov,et al.  The Tension-Stress Effect on the Genesis and Growth of Tissues , 1992 .

[19]  C. Chung,et al.  Effect of the distraction rate on the activity of the osteoblast lineage in distraction osteogenesis of rat's tibia. Immunostaining study of the proliferating cell nuclear antigen, osteocalcin, and transglutaminase C. , 1997, Bulletin (Hospital for Joint Diseases (New York, N.Y.)).

[20]  M L Samchukov,et al.  Biomechanical considerations of mandibular lengthening and widening by gradual distraction using a computer model. , 1998, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[21]  Michael T Longaker,et al.  Angiogenesis Is Required for Successful Bone Induction During Distraction Osteogenesis , 2005, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[22]  J Aronson,et al.  Temporal and spatial increases in blood flow during distraction osteogenesis. , 1994, Clinical orthopaedics and related research.

[23]  Damien Lacroix,et al.  Development of a dynamic mechano-regulation model based on shear strain and fluid flow to optimize distraction osteogenesis , 2006 .

[24]  J Y Rho,et al.  Mechanical loading thresholds for lamellar and woven bone formation , 1994, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[25]  Joyce Y. Wong,et al.  Directed Movement of Vascular Smooth Muscle Cells on Gradient-Compliant Hydrogels† , 2003 .

[26]  Ulrich S Schwarz,et al.  Physical determinants of cell organization in soft media. , 2005, Medical engineering & physics.

[27]  M Cozzani,et al.  Mechanical behavior of an osteotomized mandible with distraction orthodontic devices. , 2006, Journal of biomechanics.

[28]  I. Stokes,et al.  Endochondral growth in growth plates of three species at two anatomical locations modulated by mechanical compression and tension , 2006, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[29]  K. M. Golos,et al.  Cumulative fatigue damage , 1988 .

[30]  K. Ishizeki,et al.  Morphological characteristics of the life cycle of resting cartilage cells in mouse rib investigated in intrasplenic isografts , 2004, Anatomy and Embryology.

[31]  I. Asahina,et al.  Human osteogenic protein-1 induces both chondroblastic and osteoblastic differentiation of osteoprogenitor cells derived from newborn rat calvaria , 1993, The Journal of cell biology.

[32]  D. Paley,et al.  Variables affecting time to bone healing during limb lengthening. , 1994, Clinical orthopaedics and related research.

[33]  Rik Huiskes,et al.  Comparison of biophysical stimuli for mechano-regulation of tissue differentiation during fracture healing. , 2006, Journal of biomechanics.

[34]  M J Gómez-Benito,et al.  Influence of fracture gap size on the pattern of long bone healing: a computational study. , 2005, Journal of theoretical biology.

[35]  Jan Feijen,et al.  Micromechanical testing of individual collagen fibrils. , 2006, Macromolecular bioscience.

[36]  W. E. Roberts,et al.  Nuclear size as a cell-kinetic marker for osteoblast differentiation. , 1982, The American journal of anatomy.

[37]  J. McGahan,et al.  Deep-vein thrombosis after fracture of the pelvis: assessment with serial duplex-ultrasound screening. , 1990, The Journal of bone and joint surgery. American volume.

[38]  Z. J. Liu,et al.  Effect of distraction rate and consolidation period on bone density following mandibular osteodistraction in rats. , 2003, Archives of oral biology.

[39]  T. Gardner,et al.  The biomechanical environment of a bone fracture and its influence upon the morphology of healing. , 2003, Medical engineering & physics.

[40]  K. A. A. Ruhaimi Comparison of different distraction rates in the mandible: an experimental investigation. , 2001 .

[41]  柑本 晴夫 Bone lengthening in rabbits by callus distraction , 1988 .

[42]  J L Lewis,et al.  A composites theory predicts the dependence of stiffness of cartilage culture tissues on collagen volume fraction. , 1999, Journal of biomechanics.

[43]  Thomas A Einhorn,et al.  Effects of the local mechanical environment on vertebrate tissue differentiation during repair: does repair recapitulate development? , 2003, Journal of Experimental Biology.

[44]  K. Takaoka,et al.  Alterations in the expression of osteonectin, osteopontin and osteocalcin mRNAs during the development of skeletal tissues in vivo. , 1994, Bone and mineral.

[45]  J. Kenwright,et al.  The timing of distraction of an osteotomy. , 1990, The Journal of bone and joint surgery. British volume.

[46]  Y. Sugioka,et al.  Localization and Quantification of Proliferating Cells During Rat Fracture Repair: Detection of Proliferating Cell Nuclear Antigen by Immunohistochemistry , 1997, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[47]  T. Goto,et al.  Bone lengthening in rabbits by callus distraction. The role of periosteum and endosteum. , 1988, The Journal of bone and joint surgery. British volume.

[48]  Rik Huiskes,et al.  Bone regeneration during distraction osteogenesis: mechano-regulation by shear strain and fluid velocity. , 2007, Journal of biomechanics.

[49]  D Kaspar,et al.  Effects of Mechanical Factors on the Fracture Healing Process , 1998, Clinical orthopaedics and related research.

[50]  M J Gómez-Benito,et al.  A 3D computational simulation of fracture callus formation: influence of the stiffness of the external fixator. , 2006, Journal of biomechanical engineering.

[51]  J. Cordey,et al.  Force required for bone segment transport in the treatment of large bone defects using medullary nail fixation. , 1994, Clinical orthopaedics and related research.

[52]  P J Kelly,et al.  Permeability of cortical bone of canine tibiae. , 1987, Microvascular research.

[53]  Thomas A Einhorn,et al.  Fracture healing as a post‐natal developmental process: Molecular, spatial, and temporal aspects of its regulation , 2003, Journal of cellular biochemistry.

[54]  S. Woo,et al.  Biomechanics of knee ligaments: injury, healing, and repair. , 2006, Journal of biomechanics.

[55]  Ilizarov Ga,et al.  The principles of the Ilizarov method. , 1988 .

[56]  Michael T Longaker,et al.  Relationships between tissue dilatation and differentiation in distraction osteogenesis. , 2006, Matrix biology : journal of the International Society for Matrix Biology.

[57]  W R Walsh,et al.  Effect of Distraction Rate on Biomechanical, Mineralization, and Histologic Properties of an Ovine Mandible Model , 2000, Plastic and reconstructive surgery.

[58]  P. Dawson,et al.  A microstructural model for the anisotropic drained stiffness of articular cartilage. , 1990, Journal of biomechanical engineering.

[59]  J. Helms,et al.  Cellular and molecular characterization of a murine non‐union model , 2004, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[60]  G A Ilizarov,et al.  The tension-stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation. , 1989, Clinical orthopaedics and related research.

[61]  P J Prendergast,et al.  Biophysical stimuli on cells during tissue differentiation at implant interfaces , 1997 .

[62]  N. Sasaki,et al.  Elongation mechanism of collagen fibrils and force-strain relations of tendon at each level of structural hierarchy. , 1996, Journal of biomechanics.

[63]  Friedrich Pauwels Eine neue Theorie über den Einfluß mechanischer Reize auf die Differenzierung der Stützgewebe , 1965 .

[64]  Toshiro Ohashi,et al.  Regulation of cyclic longitudinal mechanical stretch on proliferation of human bone marrow mesenchymal stem cells. , 2007, Molecular & cellular biomechanics : MCB.

[65]  A. Simpson,et al.  Assessment of cell proliferation in regenerating bone during distraction osteogenesis at different distraction rates , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[66]  J. Weiss,et al.  Bone Regeneration and Fracture Healing: Experience With Distraction Osteogenesis Model , 1998, Clinical orthopaedics and related research.

[67]  C Ament,et al.  A fuzzy logic model of fracture healing. , 2000, Journal of biomechanics.

[68]  M. Longaker,et al.  The molecular biology of distraction osteogenesis. , 2002, Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery.

[69]  A. Simpson,et al.  TISSUES FORMED DURING DISTRACTION OSTEOGENESIS IN THE RABBIT ARE DETERMINED BY THE DISTRACTION RATE: LOCALIZATION OF THE CELLS THAT EXPRESS THE mRNAs AND THE DISTRIBUTION OF TYPES I AND II COLLAGENS , 2000, Cell biology international.

[70]  Ray Vanderby,et al.  Subfailure damage in ligament: a structural and cellular evaluation. , 2002, Journal of applied physiology.

[71]  P. Prendergast,et al.  A mechano-regulation model for tissue differentiation during fracture healing: analysis of gap size and loading. , 2002, Journal of biomechanics.

[72]  W. E. Roberts,et al.  Cell kinetics of the initial response to orthodontically induced osteogenesis in rat molar periodontal ligament , 2006, Calcified Tissue International.