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Focus Issue on Osteoporosis

Biomechanics of Osteoporosis and Vertebral Fracture

Myers, Elizabeth R., PhD; Wilson, Sara E., MS

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Abstract

From a mechanical standpoint, an osteoporotic vertebral fracture represents a structural failure of bone. Vertebral bone in the aging spine fails because it cannot support the internal stresses and strains that result from loads applied to the spine. The ability of any structure to carry load depends on several characteristics: the matter that makes up the structure and the corresponding mechanical properties of that substance, the design of the structure, and the loading conditions. In vertebrae (Figure 1), the material is predominately trabecular bone; the structural design is dictated by the shape, size, and organization of the vertebral body; and the loading conditions arise from activities of daily living and from more severe loading conditions (e.g., falls or motor vehicle trauma). With aging and osteoporosis, there are compromises in the strength of the trabecular bone and in the structural capacity of the vertebral body. In addition, loads applied to the spine may be influenced by aging of the musculo skeletal system. This article outlines the mechanical properties of vertebral bone, the structural load-carrying capacity of vertebral bodies, and the biomechanics of loads applied to the spine, each in relation to osteoporosis and risk of vertebral fracture.

Figure 1
Figure 1:
Characteristics of the spine that determine the capacity to carry load: The trabecular bone (A); the design and organization of the vertebral body (B); and the loading conditions, which are illustrated as lifting in the figure but could be any loading action (C). The depiction of trabecular bone in (A) is from microcomputed tomography of trabecular bone, a new technique for visualizing the trabecular structure.41 Panel (A) is reprinted courtesy of Ralph Müller.

Mechanical Properties of Vertebral Bone: Factors Contributing to the Strength of Trabecular Bone

Compressive forces in the spine are transferred from the intervertebral discs to the vertebral endplates and are then distributed between the trabecular centrum and the thin shell of condensed bone that make up the vertebral body. The majority of axial force is carried by the trabecular bone.25,44,45,51 Axial forces external to the vertebra, therefore, result in stresses and strains in the trabecular centrum. The ultimate strength of the trabecular bone is determined by the maximum stress that it can sustain within the overall structure of the vertebral body. The trabecular bone will fail if the strength is not greater than the working stresses in the vertebra under physiologic or traumatic conditions. Such local failures or cracks can lead to fracture of the whole bone. Strength, therefore, is an important mechanical property when considering risk of fracture.

Reductions in the apparent density of trabecular bone typify aging and osteoporosis.37 For example, direct measurements of trabecular bone density between ages 20 and 80 have shown reductions in apparent density of approximately 50%.32 In addition, results of cross-sectional studies of bone mineral density (BMD), assessed by the noninvasive technique of dual energy x-ray absorptiometry (DXA) show losses of approximately 1% per year in the spine of women more than 65 years old14 (Figure 2). It should be noted that BMD of the spine reflects apparent density of the trabecular bone and of the condensed shell and is adjusted for area rather than for volume. However, such changes in adult lumbar BMD detected by DXA reflect, in part, decreases in apparent volumetric density of the trabecular centrum.

Figure 2
Figure 2:
Age versus bone mineral density of the lumbar spine in the lateral view observed by dual-energy x-ray absorptiometry in a cross-sectional study of 120 women 65 years old or older. The correlation coefficient is r = −0.27 (P < 0.01). The negative slope indicates that lumbar bone mineral density decreases with advancing age at a rate of approximately 1% per year, although there is a great deal of variability (standard error of the regression = 0.11 g/cm2). Reproduced, with permission, from Greenspan SL, et al.14

The compressive mechanical strength of a specimen of trabecular bone is related to the apparent density squared.6,7,13,20,39 Consequently, a decrease in apparent density of the bone results in a disproportionate reduction in strength. Conversely, an increase in apparent density, as is possible with treatments for osteoporosis, could result in a beneficial effect on trabecular bone strength.

The strength of trabecular bone is also a function of the trabecular architecture, which is described by orientation, connectivity, thickness, number, and spacing of trabeculae.20 The primary architecture in the lumbar spine is characterized by horizontal and vertical trabeculae (Figure 1A). There are more vertical than horizontal trabeculae at any given density.46 Changes in the architecture of trabecular bone have been noted with the decrease in density that accompanies aging and osteoporosis. The number and thickness of the trabeculae decrease as bone density decreases in women.29,31,38,46 If the vertical trabeculae of the vertebral body represent columns supporting compressive loads and the horizontal trabeculae act as cross-struts, then thinning and loss of trabeculae would decrease the stability of the vertical columns and result in trabecular buckling.46 These alterations in trabecular architecture and reductions in density with aging and osteoporosis weaken vertebral trabecular bone substantially.

Structural Design of Vertebral Bodies: Failure Load of Human Vertebrae

Apart from the density and morphology of the trabecular bone inside a vertebra, the overall geometry of the vertebral body has an influence on the load that can be carried by the bone (Figure 1B). For instance, under compressive force, the area perpendicular to the compression axis is an important factor in the mechanical response of the structure.

In many experimental studies, the maximum force during compression of vertebral specimens from human cadavers has been assessed and the failure force related to apparent density and geometric properties of the vertebrae.5,8,25,28,30,33,47 From ages 25 to 75, the average compressive failure force changes from approximately 8000 to 2000 N in vertebrae from the thoracolumbar spine in men and women.4 The compressive failure force measured has been as low as approximately 500 N in elderly cadaveric thoracic vertebrae when the vertebra is tested with intact intervertebral discs to transfer the load.28 When measures of density and geometry are compared with failure force, strong correlation coefficients are found for human vertebrae. Bone density measured by quantitative computed tomography (QCT) times endplate area was found by Brinckmann et al5 to associate significantly with compressive failure force of thoracolumbar specimens (r = 0.8). Cody et al8 found QCT regional density values multiplied by the minimum cross-sectional area of the vertebral body to correlate strongly with lumbar failure load (multiple R2 = 0.9). More recently, DXA assessments have been used to predict vertebral failure force.28,33,47 Bone mineral density measured by DXA is the bone mineral content of a region of interest (a whole vertebral body or a subregion) divided by the projected area in the view of the DXA scan. Therefore, apparent density and geometric bone properties influence the magnitude of standard DXA measurements. Correlation coefficients for the association between lumbar BMD and failure force have ranged in results of various studies from 0.7 to 0.9, indicating that approximately 50% to 80% of the variance in failure force is explained by BMD. In results from the study by Moro et al,28 BMD of the lumbar region correlated significantly with failure force of the same lumbar vertebra tested in axial compression (r = 0.89) as well as in remote thoracic sites (r = 0.94; Figure 3).

Figure 3
Figure 3:
Bone mineral density of the second lumbar vertebral body (L2) in the lateral view versus failure force of L2 and T11 in axial compression. The correlation coefficient for L2 is r = 0.89 (P < 0.01, standard error of the regression = 730 N) and for T11 is r = 0.94 (P < 0.01, standard error of the regression = 530 N). Data are taken from Moro M et al.28

According to these results, BMD is a convenient and relatively specific method for predicting vertebral failure force under compressive loads. Furthermore, the correlation between failure force and BMD appears to be a continuum, so that there is no single "fracture threshold" value of BMD that can be used in general to identify people at risk. These studies of specimens from cadavers did not examine the influence of race on the correlation between BMD and failure force, and future work is needed to confirm correlations with race.

Under repetitive loading, a vertebra fails at lower load levels than those required to cause failure during a single application of force.4,17 This phenomenon is know as fatigue. The mechanisms for damage caused by fatigue in cortical and trabecular bone are thought to be crack initiation, crack growth, and final failure.20 Such microcracks have been observed in human vertebral bone and may contribute to decreased resistance of vertebrae to fracture.48

Loading Conditions

The strength and structural properties of the bone are only part of the biomechanics of osteoporotic fracture. Knowledge of the loading state of the bone is necessary to complete the picture. Fractures occur only when the loading on the bone results in internal stresses that exceed the strength of the bone. Therefore, it is necessary not only to know the strength of the bone and geometry of the vertebra but also to know the loads applied to the vertebral bodies.

Every activity, from sitting to walking to lifting a heavy object, creates loads on the spine. It is important to understand the activities during which vertebral fractures commonly occur to understand the loading environment. Unlike hip fractures, for which a fall has been identified as the associated event in approximately 90% of cases10,11,16,27 and which are readily identified as discrete fractures, the osteoporotic spine fracture is much more difficult to characterize. Difficulties arise when trying to assess the activities that characterize osteoporotic spine fractures, because vertebral fractures are classified by subtle vertebral deformities and reductions in height, making it difficult to recognize fractures consistently.3,12,26 There have been only a few observational studies that have assessed the events at the time of vertebral fracture in the elderly. Cooper et al9 used data extracted from a review of medical records from a 5-year study period to determine activities in a population-based sample of 341 patients with vertebral fracture. Sixteen percent of fractures were diagnosed incidentally during examination of the radiographs for other problems. Among the reviewed records, 113 of 341 (33%) indicated a fall at the time of fracture and another 29 (9%) indicated lifting. In a small hospital-based sample that used interviews with patients after diagnosis of fracture, preliminary results showed that almost 50% of acute, symptomatic vertebral fractures in people 60 years old and older occurred with a fall and approximately 20% occurred with controlled activities, including reaching, bending over, and lifting.35 Most of the remaining patients with fracture could not identify an activity or event at the time of the fracture. Thus, forces from falls and controlled activities should be analyzed to understand the biomechanics of a large portion of vertebral fractures.

Forces applied to the spine that result in osteoporotic fracture during controlled activities have only recently been investigated. Helpful tools for evaluating the magnitude of compressive loads on the spine are the lumbar models of Schultz, Andersson, and others, which were designed to evaluate development of low back pain in working adults engaged in bending and lifting actions.1,42,43 These models use optimization techniques to estimate trunk muscle forces and the compressive force on the spine. Wilson and Myers49,50 have adapted such lumbar models to the thoracic region and incorporated the geometry of the thorax of older people to estimate the forces on the vertebra during controlled activities. The forces applied to the spine at T8, T11, and L2 during various activities were calculated for a woman of 65 kg weight and 1.59 m height (values were mean values for a cohort of 120 women more than 65 years old).14,34 These activities were modeled as static events and are illustrated schematically in Figure 4. The estimated forces ranged from approximately 400 to 2100 N for the body habitus typical of an older women.

Figure 4
Figure 4:
Factor of risk for eight common activities as a function of lumbar bone mineral density. The numerator of the factor of risk was determined by models of spine loading at L2 for an elderly woman of average height and weight. The denominator was determined on the basis of correlations between lateral lumbar bone mineral density and structural capacity of the L2 vertebra. The values for lateral bone mineral density of the lumbar spine cover a wide range and go down to very low values. The t-score (number of standard deviations from the mean value for bone mineral density in young women) is approximately +1 for bone mineral density = 0.9 g/cm2 and −5 for bone mineral density = 0.4 g/cm2. Factor of risk is more than or close to 1 for low bone mineral density values (shaded area). The values for factor of risk are based on estimates and should be interpreted only to give suggestions of potentially dangerous actions.

The loading of the spine during falls is under investigation. There has been significant work on the relation of falls to age-related hip fractures.10,15,18,36 The impact force on the hip has been estimated at between 2900 and 4300 N for a sideways fall from standing height using rigid-body models and experimental fall data.21,22 These estimations depend on weight and height of the person falling and are derived from the impact velocity of the hip, the effective mass of that part of the body that is moving before impact, and the properties of the soft tissues overlying the hip. Using data from soft tissue property experiments40 and results of experimental studies of falling backward,23 the impact force on the pelvis can be estimated at between 2000 and 2500 N during a fall backward. The energy from such an impact would be expected to dissipate somewhat before it reached the thoracolumbar spine where fractures typically occur. Current research efforts are focused on improving impact models and examining the conduction of impact forces along the spine.

Another important loading mode on the spine, which may account for the large portion of vertebral fractures not associated with a specific single loading event, is repetitive loading. Based on the review of records by Cooper et al,9 approximately 50% of vertebral fractures are reported as spontaneous or are detected incidentally, and these may be related to such fatigue processes.

Factor of Risk

Low BMD is often used to indicate risk of fracture. However, BMD and the corresponding structural capacity of bone should always be considered in relation to the forces applied to the structure during physiologic conditions or during traumatic loading. Hayes et al19 suggested the use of a factor of risk to characterize the ratio of the force applied to a bone during operation divided by the force at which the bone fractures. A factor of risk higher than 1 indicates that the bone is overloaded and failure is likely. Conversely, a factor of risk much less than 1 indicates that fracture would not be likely to occur.

Factors of risk for vertebral fracture during controlled actions can exceed 1 for low levels of BMD in the spine (Figure 4). Factors of risk are the ratio of the estimated forces applied to the spine over the vertebral failure load on the basis of lumbar BMD. The denominator of the factor of risk was determined for a range of BMD values by using the linear correlations between BMD and failure load from results of tests in cadavers. Because the optimization of muscle forces and the static modeling of the activities give conservative estimates of the forces on the spine, risk factors near 1, as well as those higher than 1, can be considered dangerous. One interesting indication from the estimates of factor of risk in Figure 4 is that people with low BMD operate near a factor of risk of 1 during many activities of daily living. In women with below average BMD, factors of risk approach 1 for such activities as lifting a portable television or a toddler. For women in the very low range of BMD values, even such simple activities as tying shoes may place the spine at risk for fracture.

Biomechanical Indications for Prevention of Vertebral Fractures

Considering the correlation between bone strength and apparent density, therapies that maintain or increase apparent density but do not have an adverse effect on intrinsic tissue properties should have a positive effect on trabecular bone strength. In addition to enhancement of apparent density, treatments that affect the morphologic or geometric profile of bone should have a beneficial effect on vertebral structural capacity and consequently reduce the number of vertebral fractures.

An example of a therapy that affects strength is the bisphosphonate alendronate, which has been shown in nonhuman primates that have had ovariectomy to increase vertebral trabecular bone strength. With a regimen of 0.25 mg/kg given every 2 weeks for 2 years, the strength of lumbar vertebral cores increased compared with those in untreated controls and compared with those in placebo-treated animals with ovariectomy2 (Figure 5). The bone strength in the treated specimens depended on BMD in a manner very similar to the correlation in untreated bone, indicating that the accretion of bone in the vertebra produced by alendronate treatment contributed to bone strength comparable to that in normal bone.2 Clinical trials of oral alendronate in post-menopausal women have shown reductions in vertebral fractures from 6.2% to 3.2%.24 The beneficial effect on bone strength observed in mechanical testing in an animal model, therefore, seems to translate into reduced vertebral fracture rates in humans.

Figure 5
Figure 5:
Dependence of strength of trabecular bone cores tested in compression during treatment with alendronate. Baboons in three of the four treatment groups underwent ovariectomy and were treated with vehicle, a low dose of alendronate, or a high dose of alendronate. Animals in the fourth group had no surgery and were designated as control subjects. Animals were killed 2 years after ovariectomy. Cores were taken adjacent to the endplates from the fourth lumbar vertebra and were tested in axial compression. Results in the groups differed significantly, determined by analysis of variance (P < 0.01). Data from The Journal of Clinical Investigation 1993;92:2577-2586, with copyright permission of the American Society for Clinical Investigation.

Another approach to reducing the number of vertebral fractures comes from the observation that some fractures (approximately 10-20%) arise from activities is under the control of the person and occur because the person with low BMD operating near a factor of risk of 1 during certain actions. If preventable actions that load the vertebrae beyond safe levels are identified and those at risk are educated regarding avoidance of such actions, then such fractures may be prevented. As suggested by the outcome of the analysis of compressive loads on the spine and the resulting factors of risk (Figure 4), people with low bone density in the spine should be cautioned against lifting moderate to heavy objects or other actions - opening "stuck" windows, for example.

The biomechanics of vertebral fractures associated with falls are only now under investigation. Models of fall impact and loads to the spine must be developed to assess the loads on the spine during a fall. Future studies of falls and vertebral fracture may indicate future preventive measures to decrease the number of fractures associated with these accidental events.

Summary

Vertebral bone in the aging spine fails because it cannot support the internal stresses that result from loads applied to the spine. The strength of the trabecular bone in the vertebral centrum is determined by apparent density and by trabecular architecture. Reductions in density and thinning and loss of trabeculae result in corresponding reductions in strength.

The failure load of a whole vertebral body is determined by the strength of the trabecular bone in the centrum and by the geometric shape and organization of the vertebral body. Bone mineral density values, determined using such noninvasive techniques as DXA, have a direct, positive correlation with the compressive failure load of the vertebral body in white women and white men. Results of biomechanical studies show that assessment of BMD in vivo should indicate the peak compressive load that can be carried by the vertebral body. This correlation should be determined according to race.

The strength of bone and the load-bearing capacity should be considered in relation to the forces applied to the spine during normal activities or trauma. The ratio of loads applied to the spine during specified activities divided by the failure load of the vertebral body is the factor of risk. Factors of risk higher than 1 indicate that the load on the vertebra exceeds the structural capacity and suggest that fracture is likely to occur. To create a model of the loading conditions and determine the loads on the spine, it is necessary to understand the events that are associated with vertebral fractures. Vertebral fractures occur in a heterogeneous set of circumstances. Activities associated with some fractures include falling and controlled activities (e.g., lifting a moderate weight), but approximately 50% of vertebral fractures are not attributed to a known loading activity. For fractures resulting from controlled actions, it has been shown that everyday activities can result in factors of risk higher than 1 in people with very low vertebral BMD.

Acknowledgments

The authors thank Jeanine Dulong for help in preparing the manuscript and Ralph Müller for providing the image of trabecular bone in Figure 1A.

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Keywords:

biomechanics; bone mineral density; bone strength; osteoporosis; vertebral fracture

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