Stress-concentrating effect of resorption lacunae in trabecular bone☆
Introduction
Bone remodelling is a continuous process carried out by osteoclasts and osteoblasts in a coupled action of bone resorption and deposition. In trabecular bone osteoclasts travel along the surface of trabeculae, resorbing the tissue and forming a resorption cavity, and osteoblasts follow along behind filling in the cavity with osteoid, which subsequently mineralizes (Parfitt, 1984). It is generally agreed that this process tends to adapt the architecture of cancellous bone so that there is minimum stress in the bone tissue relative to its weight (Hart, 2001). However, it has been observed that microdamage is generated in both trabecular (Vashishth et al., 2000) and cortical bone (Lee et al., 2002) under everyday physiological loading conditions and these observations lead to the suggestion that trabecular bone remodelling may also prevent accumulation of microdamage, as has been hypothesised for compact bone (Carter et al., 1987; Frost, 1986; Martin and Burr, 1989; Prendergast and Taylor, 1994; Martin, 2002).
Because resorption cavities occurring during trabecular remodelling can be large relative to the size of the trabeculae, it is possible that significant elevations of stress occur around them. Van der Linden et al. (2001) constructed finite element models of cancellous bone at 28 μm resolution and resorption cavities were created by removing 28×28×28 μm3 volumes from the trabecular structures to create cavities 28, 56, or 84 μm deep. They observed that the presence of resorption lacunae resulted in increased strain at the base of the resorption cavity and decreased strain along the tip. However, given that resorption lacunae are typically 40–60 μm in depth, these resolutions could not give a detailed description of the consequences of resorption cavities on the strain distribution in bone tissue. For such an analysis models of individual trabeculae are required. Smit and Burger (2000) used finite element models of trabeculae assuming cylindrical geometry for the trabeculum and a hemi-spherical geometry for the Howship's lacuna on a trabecular surface. The trabeculum was loaded to produce 1000 microstrain in the longitudinal direction. They predicted increased strains both at the bottom of the lacuna and perpendicular to the direction of loading, where resorption is stopped and osteoblasts are recruited to fill the gap, and lower strains in the direction of loading, where osteoclast resorption activity continues. Based on these observations they proposed that BMU activity is regulated by strain, whereby low strains stimulate osteoclast resorption and increased strains inhibit osteoclasts and activate osteoblasts to refill. As the lacunar geometry was assumed hemi-spherical in their study, the analysis could not give information on the actual strains local to resorption cavities in vivo; such analyses would require finite element models with anatomically accurate trabecular bone geometries.
In this study, we hypothesise that bone resorption occurring during trabecular bone remodelling causes high stress concentrations in bone trabeculae. In particular we are interested to determine whether or not the stress concentrations could be of sufficient magnitude to generate damage in the bone tissue because, if it were, then damage around the resorption cavity could stimulate the continuation of the BMU activity and the travelling of a resorption pit across the trabecular surface.
Section snippets
Methods
Sections of cancellous bone from the proximal tibia, and the distal and proximal femur, of 6- and 10-month-old Whistar rats were cut under constant irrigation and were cleaned of bone marrow using a water jet. A dissecting microscope was used to locate trabecular rods, which were removed using a scalpel blade and forceps. Solid models of the microspecimens were generated using either serial sectioning and imaging at microresolutions, following the technique of Van der Linden (2002), or micro-CT
Results
The images obtained from serial sectioning were obtained at a resolution that was adequate for identifying the micro-structural geometry of trabeculae. Geometrical features such as the presumptive lacunae1 and side branching were observed in the cross-sectional images of some of the trabeculae [Fig. 4(a)].
The distributions of maximum principal stress
Discussion
In this study, we have shown that the stress/strain distribution within individual trabeculae is highly heterogeneous, even under the simplified loading conditions employed in our analysis. Furthermore it was predicted that stress and strain levels within trabeculae are elevated by the presence of what seem to be resorption lacunae. In each of the trabeculae the elevated stresses were associated with the locations of the cavities.
A number of assumptions were made in this analysis that require
Acknowledgements
Financial support provided by the European Commission Framework 6 program (Quality of Life and Management of Living Resources) project, “Mechanical Integrity and Architecture of Bone: Mechanical Integrity and Architecture of Bone Relative to Osteoporosis, Ageing and Drug Treatment (MIAB)”.
References (35)
- et al.
Changes of interstitial bone thickness with age in men and women
Bone
(1993) - et al.
Stereology and histogram analysis of backscattered electron images: age changes in bone
Bone
(1993) - et al.
Bone remodeling in response to in vivo fatigue microdamage
Journal of Biomechanics
(1985) - et al.
Trabecular bone density and loading history: regulation of connective tissue biology by mechanical energy
Journal of Biomechanics
(1987) - et al.
A comparison of the fatigue behaviour of human trabecular and cortical bone tissue
Journal of Biomechanics
(1992) - et al.
The elastic moduli of human subchondral, trabecular, and cortical bone tissue and the size-dependency of cortical bone modulus
Journal of Biomechanics
(1990) Is all cortical bone remodelling initiated by microdamage?
Bone
(2002)- et al.
Increased intracortical remodeling following fatigue damage
Bone
(1993) - et al.
Structural and material mechanical properties of human vertebral cancellous bone
Medical Engineering and Physics
(1997) - et al.
Prediction of bone adaptation using damage accumulation
Journal of Biomechanics
(1994)
Observations of microdamage around osteocyte lacunae in bone
Journal of Biomechanics
Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation
Biomaterials
Tensile testing of rodlike trabeculae excised from bovine femoral bone
Journal of Biomechanics
A new method to determine trabecular bone elastic properties and loading using micromechanical finite-element models
Journal of Biomechanics
In vivo diffuse damage in human vertebral trabecular bone
Bone
The effects of long-term hormone replacement therapy on bone remodeling in postmenopausal women
Bone
Fatigue behaviour of adult cortical bone: the influence of mean strain and strain rate
Acta Orthopedica Scandinavica
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This paper was presented, in part, at the 13th Conference of the European Society of Biomechanics (ESB), Wrocław, Poland, in September 2002, where it won the ESB Student Award for best student presentation.