Elsevier

Journal of Biomechanics

Volume 44, Issue 15, 13 October 2011, Pages 2659-2666
Journal of Biomechanics

Age-related differences in the morphology of microdamage propagation in trabecular bone

https://doi.org/10.1016/j.jbiomech.2011.08.006Get rights and content

Abstract

Microdamage density has been shown to increase with age in trabecular bone and is associated with decreased fracture toughness. Numerous studies of crack propagation in cortical bone have been conducted, but data in trabecular bone is lacking. In this study, propagation of severe, linear, and diffuse damage was examined in trabecular bone cores from the femoral head of younger (61.3±3.1 years) and older (75.0±3.9 years) men and women. Using a two-step mechanical testing protocol, damage was first initiated with static uniaxial compression to 0.8% strain then propagated at a normalized stress level of 0.005 to a strain endpoint of 0.8%. Coupling mechanical testing with a dual-fluorescent staining technique, the number and length/area of propagating cracks were quantified. It was found that the number of cycles to the test endpoint was substantially decreased in older compared to younger samples (younger: 77,372±15,984 cycles; older: 34,944±11,964 cycles, p=0.06). This corresponded with a greater number of severely damaged trabeculae expanding in area during the fatigue test in the older group. In the younger group, diffusely damaged trabeculae had a greater damage area, which illustrates an efficient energy dissipation mechanism. These results suggest that age-related differences in fatigue life of human trabecular bone may be due to differences in propagated microdamage morphology.

Introduction

Fatigue microdamage forms after repeated loading in daily activities (Burr et al., 1985). Damage formation is not necessarily pathologic; microdamage dissipates strain energy and limits the development of more serious fractures at sites subjected to high stress (Vashishth et al., 1997). Damaged sites are repaired using targeted remodeling mechanisms, preserving the structural integrity of the trabecular lattice (Burr et al., 1985). With aging, however, targeted remodeling processes diminish and allow fatigue microdamage to accumulate (Schaffler and Choi, 1995, Allen and Burr, 2008). Also, changes in trabecular matrix properties and morphology with age, including increased local mineralization levels, decreased thickness, increased spacing, loss of connectivity, and increased anisotropy, contribute to the deterioration of bone strength and stiffness and can promote microdamage formation and propagation (Burr et al., 1997). Significant damage accumulation lowers stiffness and increases the probability of fracture (Burr and Turner, 1998, Sobelman and Gibeling, 2004).

Much of what is known about age-related differences in microdamage and fatigue properties is derived from cortical (Schaffler and Choi, 1995, Vashishth and Tanner, 2000, Norman and Yeni, 1998, Zioupos, 2001a, Zioupos, 2001b) rather than trabecular bone studies (Seeman, 2003; Cook and Zioupos, 2009). Previous studies have reported that bone from younger individuals has a longer fatigue life due to increased formation of diffuse damage, whereas bone from older donors form fewer but longer linear microcracks (Diab et al., 2006). Linear microdamage, associated with a quadratic loss of modulus, propagates more easily than diffuse damage, which can dissipate energy while limiting propagation (Burr and Turner, 1998, Diab and Condon, 2006). However it is unclear whether these findings are translatable to trabecular bone.

Furthermore, it is unclear whether sex differences influence the fatigue behavior of trabecular bone. Histomorphometric studies have found few bone volume fraction or compressive strength differences attributable to sex in vertebral trabecular bone in age-matched groups (Bergot and Laval-Jeantet, 1988, Thomsen and Ebbesen, 2000, Keaveny and Yeh, 2002). One study reported an increased tendency for perforation of horizontal trabecular struts and increased trabecular spacing between horizontal trabeculae in females compared with males, but found no other histomophometric sex differences (Mosekilde, 1989). Given that 3 out of 4 fragility fractures occur in women, further investigation into sex differences in fatigue behavior is warranted.

In this study, trabecular bone cores from the femoral head of men and women aged 55–81 years were tested in a two-step mechanical testing protocol in order to investigate age and sex differences in crack propagation. We hypothesize that bone from older individuals will demonstrate decreased resistance to crack propagation, though we do not expect to see differences due to sex.

Section snippets

Methods

Femoral heads from 10 males and 10 females aged 55–81 years were obtained using the National Disease Research Interchange (NDRI). Donors had no history of bone disease, cancer, or use of medication altering bone morphology. Tissue was removed at autopsy within 12 h of death and fresh frozen at –80 °C. Donors were initially divided into four groups based on sex and age: young males (60.2±3.7 years; mean±s.d.), old males (77.2±1.5 years), young females (63.0±2.8 years), and old females (72.8±4.8

Results

No differences due to sex were noted for any comparisons, so sex groups were combined and comparisons were made between younger and older groups (younger: 61.3±3.1 years; older: 75.0±3.9 years). Gross morphological properties are reported for all mechanically tested samples (two cores/donor, n=20 per age group) and microdamage-assessed samples (one core/donor, n=10 per age group). An assessment of the global architectural properties of the trabecular bone samples revealed no significant

Discussion

In this study, trabecular bone cores from the femoral head of 10 younger and 10 older individuals were subjected to a two-step mechanical testing protocol. Microdamage was first induced with static uniaxial compressive loading to 0.8% then propagated with cyclic uniaxial compressive loading under a modest normalized stress range. It was found that samples from older donors reached the fatigue test endpoint with substantially fewer cycles than younger individuals. This was associated with

Conflict of interest statement

The authors have no conflicts of interest to disclose.

Acknowledgments

This research study was supported by NIH grant R01 AG027249. The micro-CT system was provided by NSF Major Research Instrumentation Award 9977551.

References (43)

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