Regular articleDegradation of bone structural properties by accumulation and coalescence of microcracks
Introduction
Application of cyclic strains lower than those required to fracture normal bone in a single cycle may result in partial or complete pathological fatigue or stress fracture [1]. Fatigue fractures are common in human beings, dogs, and horses [2], [3], [4], [5], [6]. Site-specific fatigue fractures associated with generalized skeletal weakening are particularly common in elderly human beings and in individuals with osteoporosis [3], [7], [8], and are also common in human, canine, and equine running athletes [2], [4], [5], [6]. There is an apparent paradox between the prevalence of these pathological fractures and the degree of fatigue resistance bone exhibits as a material [9]. Taken together, these data suggest that the structural properties of whole bones and the biological response of bone to cyclic load are likely to be key factors in the disease mechanism for fatigue fracture.
Physiological cyclic loading of the skeleton of larger mammals, such as human beings and dogs, leads to the formation of bone microcracks because of fatigue failure at the microscopic level [10], [11], and microcrack accumulation and coalescence may be an important factor leading to pathological weakening of the skeleton [7]. Interestingly, pathological fatigue fractures in running athletes usually occur through adapted actively remodeling bone [5], [12], [13], [14]. Approximately 30% of remodeling is targeted to the repair of microcracks [15], suggesting that bone porosity may be increased after the induction of microcracks, at least temporarily. Accumulation of microcracks and porosity in aged dogs, a species in which bone fracture risk remains low throughout life, is much reduced compared with aged human beings [10]. These findings suggest that both microcrack induction and the subsequent targeted remodeling response within bone may both be important determinants of bone fracture risk in life. However, the relative effects of microcracking of bone and any associated adaptation on fracture risk within whole bones are presently unclear.
The purpose of the present study was to determine the effect of fatigue loading and the associated accumulation of microcracks on whole bone structural properties ex vivo. When bone loses 15% or greater stiffness, microcrack accumulation is exponential [16], but the effect of this damage on structural properties is unclear. We, therefore, hypothesized that fatigue loading of whole bones ex vivo beyond 15% loss of stiffness would have significant effects on both induction of microcracks and whole bone structural properties. Because of the irregular shape and larger size of whole bones, it is likely that effects from the geometry and stressed volume of the specimen will influence initiation and growth of microcracks into a fracture [17].
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Experimental design
A homogeneous group of 41 adult male Sprague-Dawley rats weighing 400 to 600 g was obtained, after euthanasia had been performed for reasons unrelated to this study. The rats were stored at −20 °C until required for biomechanical testing. We used the end-loading ulnar bending model for fatigue testing (Fig. 1) [18], [19]. In this model, cyclic axial loads are applied to the antebrachium through the external surface of the olecranon and the flexed carpus via small loading cups attached to the
Results
There were no significant differences in B.Ar (P = 0.37), IMAX, (P = 0.13), IMIN (P = 0.37), and vBMD (P > 0.08) between groups. There were significant differences in vBMD between bone pairs in Groups 1 and 5 (<2% difference, P < 0.05), but not Groups 2, 3, and 4 (P > 0.29). In Groups 4 and 5, differences between fatigued and monotically tested ulnae in B.Ar (P > 0.41), and IMAX (P > 0.58) were not significant. However, small but significant differences in IMIN (10% difference, P = 0.04) were
Discussion
Fatigue fractures are an important health problem in humans and animals, particularly in the elderly, individuals with metabolic bone disease, such as osteoporosis, and in running athletes [5], [6], [7]. Although it is generally accepted that accumulation and coalescence of microcracks is an important determinant of whole bone structural properties [7], [17], this relationship is largely unstudied, and few data are available from experimental or naturally occurring fatigue fracture models [21].
Acknowledgements
This work was supported by grants from the AO Foundation, Switzerland and the Wisconsin Alumni Research Foundation, University of Wisconsin—Madison.
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