Living with cracks: damage and repair in human bone.

Our bones are full of cracks, which form and grow as a result of daily loading activities. Bone is the major structural material in our bodies. Although weaker than many engineering materials, it has one trick that keeps it ahead - it can repair itself. Small cracks, which grow under cyclic stresses by the mechanism of fatigue, can be detected and removed before they become long enough to be dangerous. This article reviews the work that has been done to understand how cracks form and grow in bone, and how they can be detected and repaired in a timely manner. This is truly an interdisciplinary research field, requiring the close cooperation of materials scientists, biologists and engineers.

[1]  B. Martin,et al.  Mathematical model for repair of fatigue damage and stress fracture in osteonal bone , 1995, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[2]  Theo H Smit,et al.  Strain-derived canalicular fluid flow regulates osteoclast activity in a remodelling osteon--a proposal. , 2003, Journal of biomechanics.

[3]  R. Heaney,et al.  Is the paradigm shifting? , 2003, Bone.

[4]  R O Ritchie,et al.  Mechanistic aspects of fracture and R-curve behavior in human cortical bone. , 2005, Biomaterials.

[5]  T. Gunnlaugsson,et al.  Detecting microdamage in bone , 2003, Journal of anatomy.

[6]  R. Martin Fatigue damage, remodeling, and the minimization of skeletal weight. , 2003, Journal of theoretical biology.

[7]  J. Nyman,et al.  Effect of ultrastructural changes on the toughness of bone. , 2005, Micron.

[8]  R O Ritchie,et al.  Effect of aging on the toughness of human cortical bone: evaluation by R-curves. , 2004, Bone.

[9]  J. Nyman,et al.  The influence of water removal on the strength and toughness of cortical bone. , 2006, Journal of biomechanics.

[10]  D. Vashishth Age-dependent biomechanical modifications in bone. , 2005, Critical reviews in eukaryotic gene expression.

[11]  R. Martin,et al.  New insights into the propagation of fatigue damage in cortical bone using confocal microscopy and chelating fluorochromes. , 2005, European journal of morphology.

[12]  E. Liao,et al.  Microcracks: an alternative index for evaluating bone biomechanical quality , 2004, Journal of Bone and Mineral Metabolism.

[13]  D. Burr,et al.  Do Bone Cells Behave Like a Neuronal Network? , 2002, Calcified Tissue International.

[14]  D. Taylor.,et al.  Scaling effects in the fatigue strength of bones from different animals. , 2000, Journal of theoretical biology.

[15]  Gerard J. Tortora,et al.  Principles of Human Anatomy , 1977 .

[16]  D B Burr,et al.  Increased intracortical remodeling following fatigue damage. , 1993, Bone.

[17]  S. Stover,et al.  Equine cortical bone exhibits rising R-curve fracture mechanics. , 2003, Journal of biomechanics.

[18]  R O Ritchie,et al.  Fracture in human cortical bone: local fracture criteria and toughening mechanisms. , 2005, Journal of biomechanics.

[19]  David Taylor,et al.  Mechanisms of short crack growth at constant stress in bone. , 2006, Biomaterials.

[20]  Jiliang Li,et al.  Imaging bone microdamage in vivo with positron emission tomography. , 2005, Bone.

[21]  R. H. Fitzgerald,et al.  Non-cemented total hip arthroplasty , 1987 .

[22]  C. M. Agrawal,et al.  Age-Related Changes of Noncalcified Collagen in Human Cortical Bone , 2003, Annals of Biomedical Engineering.

[23]  O. Verborgt,et al.  Loss of Osteocyte Integrity in Association with Microdamage and Bone Remodeling After Fatigue In Vivo , 2000, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[24]  M. Markel,et al.  Role of endochondral ossification of articular cartilage and functional adaptation of the subchondral plate in the development of fatigue microcracking of joints. , 2006, Bone.

[25]  F. O'Brien,et al.  An improved labelling technique for monitoring microcrack growth in compact bone. , 2002, Journal of biomechanics.

[26]  C. Tabin,et al.  BMP2 activity, although dispensable for bone formation, is required for the initiation of fracture healing , 2006, Nature Genetics.

[27]  D. Fyhrie,et al.  A rate-dependent microcrack-bridging model that can explain the strain rate dependency of cortical bone apparent yield strength. , 2003, Journal of biomechanics.

[28]  M G Mullender,et al.  Mechanobiology of bone tissue. , 2005, Pathologie-biologie.

[29]  Ozan Akkus,et al.  Fracture mechanics of cortical bone tissue: a hierarchical perspective. , 2004, Critical reviews in biomedical engineering.

[30]  O. Akkus,et al.  Microcracks colocalize within highly mineralized regions of cortical bone tissue. , 2005, European journal of morphology.

[31]  P Zioupos,et al.  The role of collagen in the declining mechanical properties of aging human cortical bone. , 1999, Journal of biomedical materials research.

[32]  D. Burr,et al.  A hypothetical mechanism for the stimulation of osteonal remodelling by fatigue damage. , 1982, Journal of biomechanics.

[33]  J. Currey,et al.  Mechanical properties of bone tissues with greatly differing functions. , 1979, Journal of biomechanics.

[34]  D. Taylor.,et al.  The cellular transducer in damage-stimulated bone remodelling: a theoretical investigation using fracture mechanics. , 2003, Journal of theoretical biology.

[35]  J. Nyman,et al.  A theoretical analysis of long-term bisphosphonate effects on trabecular bone volume and microdamage. , 2004, Bone.

[36]  V. Kalscheur,et al.  Aging and accumulation of microdamage in canine bone. , 2002, Bone.

[37]  N L Fazzalari,et al.  Assessment of cancellous bone quality in severe osteoarthrosis: bone mineral density, mechanics, and microdamage. , 1998, Bone.

[38]  C. Rimnac,et al.  Cortical bone tissue resists fatigue fracture by deceleration and arrest of microcrack growth. , 2001, Journal of biomechanics.

[39]  C. Rimnac,et al.  The effect of gamma radiation sterilization on the fatigue crack propagation resistance of human cortical bone. , 2004, The Journal of bone and joint surgery. American volume.

[40]  R Vanderby,et al.  Response of the osteocyte syncytium adjacent to and distant from linear microcracks during adaptation to cyclic fatigue loading. , 2004, Bone.

[41]  J. Currey,et al.  Effects of differences in mineralization on the mechanical properties of bone. , 1984, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[42]  A. Boyde The real response of bone to exercise , 2003, Journal of anatomy.

[43]  D Vashishth,et al.  Experimental validation of a microcracking-based toughening mechanism for cortical bone. , 2003, Journal of biomechanics.

[44]  A Staines,et al.  Bone adaptation to load: microdamage as a stimulus for bone remodelling , 2002, Journal of anatomy.

[45]  L. Lanyon,et al.  Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. , 2003, American journal of physiology. Cell physiology.

[46]  D P Fyhrie,et al.  Intracortical remodeling in adult rat long bones after fatigue loading. , 1998, Bone.

[47]  W. Ambrosius,et al.  Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures. , 1997, Bone.

[48]  T. Murakami,et al.  Evaluation for Mechanism of Diffuse Damage in Cortical Bone , 2005 .

[49]  C Milgrom,et al.  Aging and matrix microdamage accumulation in human compact bone. , 1995, Bone.

[50]  S. Stover,et al.  Do microcracks decrease or increase fatigue resistance in cortical bone? , 2004, Journal of biomechanics.

[51]  D. Taylor.,et al.  Microdamage and mechanical behaviour: predicting failure and remodelling in compact bone , 2003, Journal of anatomy.

[52]  D Vashishth,et al.  In vivo diffuse damage in human vertebral trabecular bone. , 2000, Bone.

[53]  P J Prendergast,et al.  Prediction of bone adaptation using damage accumulation. , 1994, Journal of biomechanics.

[54]  D. Fyhrie,et al.  The morphological association between microcracks and osteocyte lacunae in human cortical bone. , 2005, Bone.

[55]  D B Burr,et al.  Calculating the probability that microcracks initiate resorption spaces. , 1993, Journal of biomechanics.

[56]  Fergal J O'Brien,et al.  Microcrack accumulation at different intervals during fatigue testing of compact bone. , 2003, Journal of biomechanics.

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

[58]  D B Burr,et al.  Targeted and nontargeted remodeling. , 2002, Bone.

[59]  David Taylor,et al.  Microdamage: a cell transducing mechanism based on ruptured osteocyte processes. , 2006, Journal of biomechanics.

[60]  David Taylor,et al.  Fatigue of bone and bones: An analysis based on stressed volume , 1998, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[61]  S A Goldstein,et al.  A comparison of the fatigue behavior of human trabecular and cortical bone tissue. , 1992, Journal of biomechanics.

[62]  David Taylor,et al.  A crack growth model for the simulation of fatigue in bone , 2003 .

[63]  B. Noble,et al.  Bone microdamage and cell apoptosis. , 2003, European cells & materials.

[64]  M. Rashid,et al.  A mechanistic model for internal bone remodeling exhibits different dynamic responses in disuse and overload. , 2001, Journal of biomechanics.

[65]  Matthew J. Silva,et al.  In vivo skeletal imaging of 18F-fluoride with positron emission tomography reveals damage- and time-dependent responses to fatigue loading in the rat ulna. , 2006, Bone.

[66]  David Taylor,et al.  The effect of bone microstructure on the initiation and growth of microcracks , 2005, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.