Elsevier

Bone

Volume 30, Issue 5, May 2002, Pages 759-764
Bone

Original article
Cancellous bone mechanical properties from normals and patients with hip fractures differ on the structure level, not on the bone hard tissue level

https://doi.org/10.1016/S8756-3282(02)00693-2Get rights and content

Abstract

Osteoporosis is currently defined in terms of low bone mass. However, the source of fragility leading to fracture has not been adequately described. In particular, the contributions of bone tissue properties and architecture to the risk or incidence of fracture are poorly understood. In an earlier experimental study, it was found that the architectural anisotropy of cancellous bone from the femoral heads of fracture patients was significantly increased compared with age- and density-matched control material (Ciarelli et al., J Bone Miner Res 15:32–40; 2000). Using a combination of compression testing and micro-finite element analysis on a subset of cancellous bone specimens from that study, we calculated the hard tissue mechanical properties and the apparent (macroscopic) mechanical properties. The tissue modulus was 10.0 GPa (SD 2.2) for the control group and 10.8 GPa (SD 3.3) for the fracture group (not significant). There were no differences in either the apparent yield strains, percentages of highly strained tissue, or the relationship between apparent yield stress and apparent elastic modulus. Hence, a difference in the tissue yield properties is unlikely. At the apparent level, the fracture group had a significantly decreased transverse stiffness, resulting in increased mechanical anisotropy. These changes suggest that bone in the fracture group was “overadapted” to the primary load axis, at the cost of fragility in the transverse direction. We conclude that individuals with a history of osteoporotic fractures do not have weaker bone tissue. Architectural and mechanical anisotropy alone renders their bone weaker in the nonprimary loading direction.

Introduction

Osteoporosis is a bone disease defined by low bone density, associated with microarchitectural deterioration of bone.9 Osteoporotic fractures are caused by an imbalance between mechanical strength of bones and the mechanical loads placed on them. Fractures due to osteoporosis occur throughout the human body, but the sites most at risk are the hip, the vertebrae, and the distal radius. The lifetime risk of a fracture at any of these three sites in 50-year-old individuals is 40% for white women and 13% for white men.5, 33

It has been shown that the stress distribution in the proximal femur during a fall to the side is dependent on the location within the femur. The percentage of the load carried by the cancellous bone varied from as little as 4% at the base of the neck to as much as 70% in the supcapital region.30 This suggests that both the cortical bone and the cancellous bone play an important role in the occurrence of hip fractures. Histological studies of the cortical bone of the proximal femur have shown that patients with hip fractures have thinner cortices.1, 4 These same studies have shown no difference in the bone density of the cancellous bone. However, this does not rule out any changes in the mechanical properties. Although volume fraction is a potent estimator of mechanical properties, it cannot clearly discriminate between bone from individuals with and without fractures.32 The mechanical properties of cancellous bone (apparent properties, order: 100 mm) depend on its morphology (volume fraction and architecture) and on the mechanical properties of its constituent tissue (tissue properties, order: 10−2 mm). Experimental studies have revealed that bone density (volume fraction) can explain up to 70% of the variance in mechanical properties,10, 22 whereas bone volume fraction and architectural parameters together can explain >90% of the variance.10, 19, 44 Recently, Ciarelli et al.3 examined cancellous bone from age-matched women with and without femoral neck fractures, whose bone mass measures overlapped, to determine if any architectural or mechanical differences were present. Architectural parameters such as trabecular number, connectivity, and thickness were not significantly different between the groups. The maximal elastic modulus and ultimate stress in the inferosuperior direction were also the same. The only difference found was a significantly greater architectural anisotropy in the fracture group.

An explanation for increased fracture risk may be a decrease in stiffness and strength of the bone tissue material itself. A number of studies concerning tissue properties of individuals with and without fractures have been published.8, 21, 28, 31, 34 Their results suggest that, in a fracture group, the average tissue density is either unchanged or slightly decreased, and that the number of microcracks in the tissue is unchanged. Both effects may reduce the mechanical properties of the tissue material. To determine whether the mechanical tissue properties were actually reduced, we extended the work of Ciarelli et al.3 First, to determine the tissue mechanical properties we used micro-finite element analysis combined with compression testing.6, 18, 20, 27, 36, 43 Second, we calculated the mechanical anisotropy from the same specimens, to determine whether this differed between those with and without fracture.

Section snippets

Materials

We used the specimens from the “equal bone mass subset” of Ciarelli et al.3 A subset that included specimens with a bone volume fraction less than one standard deviation from the mean of the fracture group, resulting in 11 control specimens (mean age 80 years, SD 12) and 19 fracture specimens (mean age 81 years, SD 8). Specimens came either from women who had undergone arthroplasty for neck fractures of the proximal femur (fracture group), or from female cadavers (control group). Specimens were

Results

The bone volume fractions for the samples were 17% (SD 2%) for the control group and 18% (SD 3%) for the fracture group (Table 1). This difference was not significant (p = 0.350, Student’s t-test). There were no significant differences between the two groups for any of the parameters measured in the compression tests (apparent modulus, apparent yield stress, and apparent yield strain; Table 1).

Discussion

We determined and compared the tissue and apparent mechanical properties of cancellous bone specimens from women with similar ages and bone densities, with and without femoral neck fractures. To this end, we combined μFEA and mechanical tests.

From the μFEA, in combination with the compression tests, we estimated the tissue elastic modulus to be slightly over 10 GPa for both groups. This value falls well within the range of values found previously for healthy bone, using experimental techniques

Acknowledgements

The authors acknowledge the contributions of the Dutch National Computing Facilities Foundation (NCF), the National Institutes of Health (USA) (AR34399), and the University of Michigan Rackham School of Graduate Studies. The contribution of Harrie Weinans was made possible by a fellowship from the Royal Netherlands Academy of Arts and Sciences.

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