The influence of collagen fiber orientation and other histocompositional characteristics on the mechanical properties of equine cortical bone

SUMMARY This study examined relative influences of predominant collagen fiber orientation (CFO), mineralization (% ash), and other microstructural characteristics on the mechanical properties of equine cortical bone. Using strain-mode-specific (S-M-S) testing (compression testing of bone habitually loaded in compression; tension testing of bone habitually loaded in tension), the relative mechanical importance of CFO and other material characteristics were examined in equine third metacarpals (MC3s). This model was chosen since it had a consistent non-uniform strain distribution estimated by finite element analysis (FEA) near mid-diaphysis of a thoroughbred horse, net tension in the dorsal/lateral cortices and net compression in the palmar/medial cortices. Bone specimens from regions habitually loaded in tension or compression were: (1) tested to failure in both axial compression and tension in order to contrast S-M-S vs non-S-M-S behavior, and (2) analyzed for CFO, % ash, porosity, fractional area of secondary osteonal bone, osteon cross-sectional area, and population densities of secondary osteons and osteocyte lacunae. Multivariate multiple regression analyses revealed that in S-M-S compression testing, CFO most strongly influenced total energy (pre-yield elastic energy plus post-yield plastic energy); in S-M-S tension testing CFO most strongly influenced post-yield energy and total energy. CFO was less important in explaining S-M-S elastic modulus, and yield and ultimate stress. Therefore, in S-M-S loading CFO appears to be important in influencing energy absorption, whereas the other characteristics have a more dominant influence in elastic modulus, pre-yield behavior and strength. These data generally support the hypothesis that differentially affecting S-M-S energy absorption may be an important consequence of regional histocompositional heterogeneity in the equine MC3. Data inconsistent with the hypothesis, including the lack of highly longitudinal collagen in the dorsal-lateral `tension' region, paradoxical histologic organization in some locations, and lack of significantly improved S-M-S properties in some locations, might reflect the absence of a similar habitual strain distribution in all bones. An alternative strain distribution based on in vivo strain measurements, without FEA, on non-Thoroughbreds showing net compression along the dorsal-palmar axis might be more characteristic of the habitual loading of some of the bones that we examined. In turn, some inconsistencies might also reflect the complex torsion/bending loading regime that the MC3 sustains when the animal undergoes a variety of gaits and activities, which may be representative of only a portion of our animals, again reflecting the possibility that not all of the bones examined had similar habitual loading histories.

[1]  J. Robertson,et al.  Nephrosplenic entrapment in the horse: a retrospective study of 174 cases. , 2010, Equine veterinary journal. Supplement.

[2]  G. Reilly,et al.  Postexercise and positional variation in mechanical properties of the radius in young horses. , 2010, Equine veterinary journal.

[3]  D Vashishth,et al.  Damage mechanisms and failure modes of cortical bone under components of physiological loading , 2005, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[4]  Steven M. Tommasini,et al.  Relationship Between Bone Morphology and Bone Quality in Male Tibias: Implications for Stress Fracture Risk , 2005, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[5]  M. Markel,et al.  Up-regulation of site-specific remodeling without accumulation of microcracking and loss of osteocytes. , 2005, Bone.

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

[7]  K. Hunt,et al.  Does the degree of laminarity correlate with site‐specific differences in collagen fibre orientation in primary bone? An evaluation in the turkey ulna diaphysis , 2004, Journal of anatomy.

[8]  K. Hunt,et al.  Relationships of loading history and structural and material characteristics of bone: Development of the mule deer calcaneus , 2004, Journal of morphology.

[9]  J. Currey The many adaptations of bone. , 2003, Journal of biomechanics.

[10]  D. Lieberman,et al.  Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs , 2003, Journal of Experimental Biology.

[11]  Alan Boyde,et al.  Circularly polarized light standards for investigations of collagen fiber orientation in bone. , 2003, Anatomical record. Part B, New anatomist.

[12]  A. Boyde,et al.  Intrapopulation variability in mineralization density at the human femoral mid‐shaft , 2003, Journal of anatomy.

[13]  Kent N Bachus,et al.  Are uniform regional safety factors an objective of adaptive modeling/remodeling in cortical bone? , 2003, Journal of Experimental Biology.

[14]  R. Martin,et al.  Fatigue Microdamage as an Essential Element of Bone Mechanics and Biology , 2003, Calcified Tissue International.

[15]  S. Stover,et al.  Osteon pullout in the equine third metacarpal bone: Effects of ex vivo fatigue , 2003, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[16]  R. T. Hart,et al.  Characterization of dynamic three-dimensional strain fields in the canine radius. , 2002, Journal of biomechanics.

[17]  C. Lovejoy,et al.  Collagen fiber orientation in the femoral necks of apes and humans: do their histological structures reflect differences in locomotor loading? , 2002, Bone.

[18]  D. Burr The contribution of the organic matrix to bone's material properties. , 2002, Bone.

[19]  J H Keyak,et al.  Stiff and strong compressive properties are associated with brittle post‐yield behavior in equine compact bone material , 2002, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[20]  C. M. Agrawal,et al.  The role of collagen in determining bone mechanical properties , 2001, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[21]  D. B. Burr,et al.  Shear Strength and Fatigue Properties of Human Cortical Bone Determined from Pure Shear Tests , 2001, Calcified Tissue International.

[22]  C. Rubin,et al.  Measurement of Bone Deformations Using Strain Gauges , 2001 .

[23]  D. Vashishth,et al.  Estimation of bone matrix apparent stiffness variation caused by osteocyte lacunar size and density. , 2001, Journal of biomechanical engineering.

[24]  D. Nunamaker Bucked Shins in Horses , 2000 .

[25]  Charles Milgrom,et al.  The Role of Strain and Strain Rates in Stress Fractures , 2000 .

[26]  C. Milgrom,et al.  Musculoskeletal fatigue and stress fractures , 2000 .

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

[28]  G. Reilly,et al.  Observations of microdamage around osteocyte lacunae in bone. , 2000, Journal of biomechanics.

[29]  D Vashishth,et al.  Decline in osteocyte lacunar density in human cortical bone is associated with accumulation of microcracks with age. , 2000, Bone.

[30]  Y. Yeni,et al.  Fracture toughness is dependent on bone location--a study of the femoral neck, femoral shaft, and the tibial shaft. , 2000, Journal of biomedical materials research.

[31]  G. Reilly,et al.  The effects of damage and microcracking on the impact strength of bone. , 2000, Journal of biomechanics.

[32]  D Vashishth,et al.  Bone stiffness predicts strength similarly for human vertebral cancellous bone in compression and for cortical bone in tension. , 2000, Bone.

[33]  P. Muir,et al.  In vivo matrix microdamage in a naturally occurring canine fatigue fracture. , 1999, Bone.

[34]  J. Currey,et al.  What determines the bending strength of compact bone? , 1999, The Journal of experimental biology.

[35]  A. Bailey,et al.  Age-Related Changes in the Biochemical Properties of Human Cancellous Bone Collagen: Relationship to Bone Strength , 1999, Calcified Tissue International.

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

[37]  G. Reilly,et al.  The development of microcracking and failure in bone depends on the loading mode to which it is adapted. , 1999, The Journal of experimental biology.

[38]  T. Wright,et al.  Collagen and Bone Strength , 1999, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[39]  D B Burr,et al.  Elastic anisotropy and collagen orientation of osteonal bone are dependent on the mechanical strain distribution , 1999, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[40]  D P Fyhrie,et al.  Damage type and strain mode associations in human compact bone bending fatigue , 1998, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[41]  A. Goodship,et al.  Exercise of young thoroughbred horses increases impact strength of the third metacarpal bone , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[42]  P. Benum,et al.  In vivo measurements show tensile axial strain in the proximal lateral aspect of the human femur , 1997, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[43]  Y. Yeni,et al.  The influence of bone morphology on fracture toughness of the human femur and tibia. , 1997, Bone.

[44]  P Zioupos,et al.  The effects of ageing and changes in mineral content in degrading the toughness of human femora. , 1997, Journal of biomechanics.

[45]  J H Keyak,et al.  The distribution of material properties in the equine third metacarpal bone serves to enhance sagittal bending. , 1997, Journal of biomechanics.

[46]  S. Stover,et al.  Residual strength of equine bone is not reduced by intense fatigue loading: implications for stress fracture. , 1997, Journal of biomechanics.

[47]  V. A. Gibson,et al.  Collagen fiber organization is related to mechanical properties and remodeling in equine bone. A comparison of two methods. , 1996, Journal of biomechanics.

[48]  R. Bloebaum,et al.  Evidence of structural and material adaptation to specific strain features in cortical bone , 1996, The Anatomical record.

[49]  D B Burr,et al.  Resistance to crack growth in human cortical bone is greater in shear than in tension. , 1996, Journal of biomechanics.

[50]  V. A. Gibson,et al.  Osteonal structure in the equine third metacarpus. , 1996, Bone.

[51]  L Cristofolini,et al.  Mechanical validation of whole bone composite femur models. , 1996, Journal of biomechanics.

[52]  R. Bloebaum,et al.  Evidence of strain-mode-related cortical adaptation in the diaphysis of the horse radius. , 1995, Bone.

[53]  R. Pidaparti,et al.  The anisotropy of osteonal bone and its ultrastructural implications. , 1995, Bone.

[54]  A. Boyde,et al.  Pattern of collagen fiber orientation in the ovine calcaneal shaft and its relation to locomotor‐induced strain , 1995, The Anatomical record.

[55]  A A Biewener,et al.  Structural response of growing bone to exercise and disuse. , 1994, Journal of applied physiology.

[56]  R. Martin,et al.  The effects of collagen fiber orientation, porosity, density, and mineralization on bovine cortical bone bending properties. , 1993, Journal of biomechanics.

[57]  J A McGeough,et al.  Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure. , 1993, The Journal of bone and joint surgery. American volume.

[58]  C H Turner,et al.  Basic biomechanical measurements of bone: a tutorial. , 1993, Bone.

[59]  L. Lanyon,et al.  Functional associations between collagen fibre orientation and locomotor strain direction in cortical bone of the equine radius , 1993, Anatomy and Embryology.

[60]  L. Lanyon,et al.  Mechanical implications of collagen fibre orientation in cortical bone of the equine radius , 1993, Anatomy and Embryology.

[61]  S. Stover,et al.  Histological features of the dorsal cortex of the third metacarpal bone mid-diaphysis during postnatal growth in thoroughbred horses. , 1992, Journal of anatomy.

[62]  C T Rubin,et al.  Characterizing bone strain distributions in vivo using three triple rosette strain gages. , 1992, Journal of biomechanics.

[63]  G. Evans,et al.  The response of equine cortical bone to loading at strain rates experienced in vivo by the galloping horse. , 1992, Equine veterinary journal.

[64]  N. Gjerdet,et al.  AGE-DEPENDENT MECHANICAL PROPERTIES OF RAT FEMUR. MEASURED IN VIVO AND IN VITRO , 1991 .

[65]  J. Bertram,et al.  THE ‘LAW OF BONE TRANSFORMATION’: A CASE OF CRYING WOLFF? , 1991, Biological reviews of the Cambridge Philosophical Society.

[66]  N. Gjerdet,et al.  Age-dependent mechanical properties of rat femur. Measured in vivo and in vitro. , 1991, Acta orthopaedica Scandinavica.

[67]  P. Haghighi,et al.  Structure, function and adaptation of compact bone , 1989, Skeletal Radiology.

[68]  C. Turner,et al.  Yield behavior of bovine cancellous bone. , 1989, Journal of biomechanical engineering.

[69]  B. Vértessy,et al.  The perfection of substrate-channelling in interacting enzyme systems: energetics and evolution. , 1988, Journal of theoretical biology.

[70]  A Ascenzi,et al.  The micromechanics versus the macromechanics of cortical bone--a comprehensive presentation. , 1988, Journal of biomechanical engineering.

[71]  J. Bertram,et al.  Bone curvature: sacrificing strength for load predictability? , 1988, Journal of theoretical biology.

[72]  R. Bloebaum,et al.  A polymethyl methacrylate method for large specimens of mineralized bone with implants. , 1987, Stain technology.

[73]  J. Bertram,et al.  Bone modeling during growth: Dynamic strain equilibrium in the chick tibiotarsus , 1986, Calcified Tissue International.

[74]  C. Ruff,et al.  Structural and mechanical indicators of limb specialization in primates. , 1985, Folia primatologica; international journal of primatology.

[75]  W C Hayes,et al.  The effect of prolonged physical training on the properties of long bone: a study of Wolff's Law. , 1981, The Journal of bone and joint surgery. American volume.

[76]  W. Hayes,et al.  Relations between tensile impact properties and microstructure of compact bone , 1977, Calcified Tissue Research.

[77]  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.

[78]  L. Lanyon,et al.  Mechanical function as an influence on the structure and form of bone. , 1976, The Journal of bone and joint surgery. British volume.

[79]  K. Heiple,et al.  Contribution of collagen and mineral to the elastic-plastic properties of bone. , 1975, The Journal of bone and joint surgery. American volume.

[80]  A. Burstein,et al.  The Mechanical Properties of Cortical Bone , 1974 .

[81]  F. G. Evans,et al.  Relations among mechanical properties, collagen fibers, and calcification in adult human cortical bone. , 1971, Journal of biomechanics.

[82]  F. G. Evans,et al.  Relation of collagen fiber orientation to some mechanical properties of human cortical bone. , 1969, Journal of biomechanics.

[83]  John D. Currey,et al.  Stress Concentrations in Bone , 1962 .

[84]  S. Stover,et al.  Osteonal effects on elastic modulus and fatigue life in equine bone. , 2006, Journal of biomechanics.

[85]  J. Currey Can strains give adequate information for adaptive bone remodeling? , 2006, Calcified Tissue International.

[86]  A. Biewener Safety factors in bone strength , 2005, Calcified Tissue International.

[87]  R. Evans,et al.  Osteocyte death and hip fracture , 2005, Calcified Tissue International.

[88]  L. Lanyon Osteocytes, strain detection, bone modeling and remodeling , 2005, Calcified Tissue International.

[89]  MICROSTRAIN FIELDS IN CORTICAL BONE IN UNIAXIAL TENSION + , 2003 .

[90]  R. Martin,et al.  Is all cortical bone remodeling initiated by microdamage? , 2002, Bone.

[91]  THE ROLE OF OSTEOCYTE LACUNA POPULATION DENSITY ON THE MECHANICAL PROPERTIES OF CORTICAL BONE , 2002 .

[92]  S. Stover,et al.  FATIGUE CRACK GROWTH RATES IN EQUINE CORTICAL BONE , 2000 .

[93]  J. Currey Why aren’t Skeletal Tissues Perfect? , 1999 .

[94]  P Zioupos,et al.  Changes in the stiffness, strength, and toughness of human cortical bone with age. , 1998, Bone.

[95]  B. Mccreadie,et al.  Strain Concentrations Surrounding an Ellipsoid Model of Lacunae and Osteocytes. , 1997, Computer methods in biomechanics and biomedical engineering.

[96]  D B Burr,et al.  Bone, exercise, and stress fractures. , 1997, Exercise and sport sciences reviews.

[97]  D. Carter,et al.  Cyclic mechanical property degradation during fatigue loading of cortical bone. , 1996, Journal of biomechanics.

[98]  A. Boyde,et al.  Macroscopic shape of, and lamellar distribution within, the upper limb shafts, allowing inferences about mechanical properties. , 1991, Bone.

[99]  A. Boyde,et al.  The quantitative study of the orientation of collagen in compact bone slices. , 1990, Bone.

[100]  R. Martin,et al.  The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. , 1989, Journal of biomechanics.

[101]  N. R. Deuel,et al.  Laterality in the gallop gait of horses. , 1987, Journal of biomechanics.

[102]  A. Boyde,et al.  On the structural symmetry of human femurs. , 1987, Bone.

[103]  W. L. Haworth,et al.  A fractographic study of human long bone. , 1986, Journal of biomechanics.

[104]  J. Russ Practical Stereology , 1986, Springer US.

[105]  R. Martin Porosity and specific surface of bone. , 1984, Critical reviews in biomedical engineering.

[106]  A. Boyde,et al.  Collagen orientation in compact bone: II. Distribution of lamellae in the whole of the human femoral shaft with reference to its mechanical properties. , 1984, Metabolic bone disease & related research.

[107]  Martin Rb Porosity and specific surface of bone. , 1984 .

[108]  A. Biewener,et al.  Bone stress in the horse forelimb during locomotion at different gaits: a comparison of two experimental methods. , 1983, Journal of biomechanics.

[109]  L E Lanyon,et al.  The relationship of functional stress and strain to the processes of bone remodelling. An experimental study on the sheep radius. , 1979, Journal of biomechanics.

[110]  W H Harris,et al.  Proximal strain distribution in the loaded femur. An in vitro comparison of the distributions in the intact femur and after insertion of different hip-replacement femoral components. , 1978, The Journal of bone and joint surgery. American volume.

[111]  D D Moyle,et al.  Work to fracture of canine femoral bone. , 1978, Journal of biomechanics.

[112]  M Martens,et al.  Aging of bone tissue: mechanical properties. , 1976, The Journal of bone and joint surgery. American volume.

[113]  W C Hayes,et al.  Fatigue life of compact bone--I. Effects of stress amplitude, temperature and density. , 1976, Journal of biomechanics.

[114]  Burton J. Bogitsh,et al.  A COMPARISON OF TWO METHODS , 1975 .

[115]  F. G. Evans,et al.  Relations of the compressive properties of human cortical bone to histological structure and calcification. , 1974, Journal of biomechanics.

[116]  F. G. Evans,et al.  Differences and relationships between the physical properties and the microscopic structure of human femoral, tibial and fibular cortical bone , 1967 .