Biomechan Model Mechanobiol (2007) 6:275285 DOI 10.

1007/s10237-006-0055-9

O R I G I NA L PA P E R

Modelling external bone adaptation using evolutionary structural optimisation

G. Chen G. J. Pettet M. Pearcy D. L. S. McElwain

Received: 6 December 2005 / Accepted: 31 May 2006 / Published online: 25 August 2006 Springer-Verlag 2006

Abstract External remodelling is signicant in the bone healing process, and it is essential to predict the bone external shape in the design of articial bone grafts. This paper demonstrates the effectiveness of the evolutionary structural optimisation (ESO) method for the simulation of bone morphology. A two-dimensional ESO strategy is developed which is capable of nding the modied bone topology beginning with any geometry under any loading conditions. The morphology of bone structure is described by the quantitative bone adaptation theory, which is integrated with the nite element method. The evolutionary topology optimisation process is introduced to nd the bone shape. A rectangle, which occupies a larger space than the external shape of the bone structure, is specied as a design domain; the evolutionary process iteratively eliminates and redistributes material throughout the domain to obtain an optimum arrangement of bone materials. The technique has been tested on a wide range of examples. In this paper, the formation of trabecular bone architecture around an implant is studied; as another example, the growth of the coronal section of a vertebral body
G. Chen (B) G. J. Pettet D. L. S. McElwain Applied Mathematics and Advanced Computation Program, School of Mathematical Sciences, Queensland University of Technology, GPO Box 2434, Brisbane, QLD 4001, Australia e-mail: g3.chen@qut.edu.au G. J. Pettet e-mail: g.pettet@qut.edu.au D. L. S. McElwain e-mail: s.mcelwain@qut.edu.au M. Pearcy School of Engineering Systems, Queensland University of Technology, GPO Box 2434, Brisbane, QLD 4001, Australia e-mail: m.pearcy@qut.edu.au

is predicted. The examples support the assertion that the external shape of bone structure can be successfully predicted by the proposed ESO procedure. Keywords Bone remodelling Topology optimisation Finite element analysis Vertebra Implant

1 Introduction A bone has the ability to adapt its external shape and internal structure to variations in its mechanical environment. The adaptive response of bones to changes in load history is called bone remodelling (Mundy 1999; Wolff 1892). A decrease in mechanical load causes resorption of bones, whereas an increase leads to bone formation. There are two types of remodelling: internal and external (Cowin and Van Buskirk 1979). External (or surface) remodelling is one which results in a change of the external shape of the overall bone structure. This occurs by the resorption or deposition of bone material on the surfaces. Internal remodelling refers to the resorption or deposition of bone material only; a change in overall shape will not result from internal remodelling, but there will be changes in the porosity, mineral content and total weight of the living bone. Internal remodelling includes the removal and densication of the architecture of cancellous bone. Following the qualitative observations of Wolff (1892), several investigators (Beaupre et al. 1990; Carter et al. 1987, 1989; Cowin and Hegedus 1976; Frost 1987; Hegedus and Cowin 1976; Huiskes et al. 1987) tried to describe the remodelling process mathematically. The complete mathematical model of bone remodelling was

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initiated by Cowin and Hegedus (1976), based on general continuum mechanics principles. In it, a bone is considered as an elastic porous medium and the bone density evolution rate is related to the difference between the actual strain and a reference value of the strain. The computational implementation of bone remodelling using a nite element model was pioneered by Hart et al. (1984) and followed by Weinans et al. (1992, 1997) and Van Rietbergen (1993). Bone remodelling theories have been successfully applied to the study of the remodelling behaviour of the proximal femur (Weinans et al. 1992) and total hip replacement (van Rietbergen et al. 1993). Huiskes et al. (1987) introduced a different remodelling algorithm which includes a lazy zone. It was assumed that bone remodelling could occur if the stimulus was either above a certain level or below a certain threshold and in between these two levels the bone structure was maintained. A bone undergoes morphological changes in response to mechanical loads by modifying its external geometry as well as its internal structure, i.e., external and internal remodelling happens simultaneously. However, for an adult person, the geometry changes are minimal in comparison with the internal change. For this reason, most published research discusses the internal remodelling process in detail (Garcia et al. 2002). However, external remodelling is important in some cases, for instance, in the bone healing process. Huiskes et al. (1987) incorporated both external and internal remodelling into a new model and pointed out the similarity between bone remodelling and adaptive shape optimisation; Luo et al. (1999) used a Boundary Element Method to study external remodelling of bony structure surrounding a cylindrical implant. Mattheck et al. (1991, 2003) used optimisation methods to study the growth of bony structures and trees. Recently, Ruimerman et al. (2005) investigated both the adaptation of density and the morphology of trabecular bone. As pointed out by many investigators (Carter et al. 1987; Harrigan and Hamilton 1994; Mullender et al. 1994), the bone is a self-organizing material, and the density distribution within a bone is optimized with respect to the external loads. Hence the bone remodelling process is an optimisation procedure, forming or resorbing bone to minimize the material mass. This self-organizing process is similar to the evolutionary topology optimisation idea in engineering (Xie and Steven 1997). Topology optimisation techniques were introduced to predict the external shapes of bone structures (Xinghua et al. 2005). The topology optimisation developed in structural engineering can be used in formnding for complex structures (Xie et al. 2005). There are two groups of procedures for carrying out topology

optimisation: the more intuitive evolutionary methods (Xie and Steven 1993) and more mathematically rigorous homogenization methods (Bendsoe and Kikuchi 1988). These two groups of methods were reviewed in Hinton (1998) and Hassani and Hinton (1998). The evolutionary methods use a uniform regular topology (a rectangle for 2D and a hexahedron for 3D) as a design domain which occupies a larger space than the external shape of the real structures, and the evolutionary process iteratively eliminates and redistributes material throughout the domain to obtain an optimum arrangement of materials. By importing the idea of topology optimisation in engineering, this paper proposes a numerical methodology that will accurately predict bone external remodelling. The basic strategy is to apply the topology optimisation techniques developed in structural engineering (Xie and Steven 1997) to bone remodelling. The remodelling process involves iteration. At each iteration, a nite element analysis is conducted to determine stresses and the bone density, and the inefcient elements are removed. The numerical methodology is applied to the formation of trabecular bone architecture around an implant. As another example of numerical validation, the growth of a vertebral body is studied in a 2D model of its coronal section.

2 Methods Bone remodelling is a complicated process. The rate of remodelling is related to the mechanical stimulus (Cowin and Hegedus 1976; Huiskes et al. 1987). In turn, the mechanical stimulus is dependent on the remodelling process. The mechanical stimulus may be characterized by the stress or the strain energy density. Hence, the prediction of bone remodelling is fully coupled with stress analysis. As pointed out by Jacobs et al. (1995), there is a similarity between the remodelling process and a fully coupled thermal-stress analysis. Any commercial nite element package, which can solve thermo-mechanics problems with temperature-dependent material properties, can be used to deal with bone remodelling by using the density in place of temperature and we adopt this approach here by using the density in place of temperature. The results produced in this paper were obtained using ABAQUS. 2.1 Bone remodelling It is well-known that the bone has sensors, which detect a mechanical stimulus and, depending on the magnitude of this stimulus, cause local bone adaptations (Mullender

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et al. 1994). This process can be described with a generic mathematical expression, using the apparent density as the characterization of the bone morphology. For the sake of simplicity, the lazy zone concept is not incorporated in the simulation, even though there are good biological reasons for supposing that a lazy zone exists. It is assumed that this stimulus is directly related to the local mechanical load in the bone and can be determined from the local stress tensor and the strain tensor. The rate of change of the apparent density of the bone at a particular location d/dt can be specied by d =B dt S k , 0 < max , (1)

2.2 Evolutionary topology optimisation The class of problems where the denition of the shape forms part of the design problem is known as topology optimisation (Payten et al. 1998). In this paper, this idea is followed and the external shape and internal structure of the actual bone are simulated from a regular design domain. Compared with homogenization methods, evolutionary structural optimisation (ESO) methods are more intuitive and easy to implement. In this paper, an ESO methodology is developed. The ESO procedure is such that each iteration consists of a nite element analysis (to determine stresses) followed by the removal of inefcient elements. The process is summarized as follows: (1) Execute a nite element analysis (ABAQUS was used here) and output element stresses and strains; (2) Dene mechanical stimulus using a remodelling theory. In this paper, the strain energy density is employed: S= 1 ; 2 (3)

where B is a constant which characterizes the remodelling speed, max is the maximum density of a bone, S = S(x, y, z) is the mechanical stimulus and k = k(x, y, z) is a reference value for remodelling. When the right side of Eq. (1) is zero, the system is in equilibrium and the net rate of change of bone-density is zero. It should be noted that the overall bone characteristics are determined by the architectural properties and material properties. The architectural properties are related to porosity and material properties are related to the degree of mineralisation of the bone. In this article the term material properties refers to the overall bone characteristics at the structural level. The bone density means the apparent density (Currey 2002), which can be changed either by modifying its porosity or its mineralisation. Cowin and Hegedus (1976) proposed a relationship in which the individual components of the actual strain tensor were considered as stimuli. Huiskes et al. (1987) used a similar approach, but the strain energy density (SED) was assumed to be the stimulus. Following Huiskes et al., this article uses SED as the stimulus. A difference between the actual SED and a reference SED at the same location would then be the driving force for adaptation of the density. Hence, in Eq. (1), S = S(x, y, z) would be the actual SED and k = k(x, y, z), the reference SED. The relation between the Youngs modulus of a bone and its density is assumed to be E=C
r

where and are stress and strain tensors, respectively; (3) Calculate the distribution of the density of bone by Euler Forward method applied to the bone remodelling Eq. (1); (4) Find the maximum and minimum values of bone density, max and min over all elements in the design domain; (5) Find the threshold value of bone density (th) = min((th1) , (th2) ); with (th1) = RR max (th2) = min + VR (max min ) (5) (4)

(2)

where C is a constant, and r = 1, 2, or 3. Carter and Hayes (1977) suggested that the exponent is about 3; Rice et al. (1988) showed that the exponent is about 2. Yang et al. (1998) conrmed that the exponent is nearer 2 than 3. A good review on mechanical properties of cancellous bone is seen in Currey (2002). In this paper, a quadratic modulus-density function is employed, i.e., r = 2.

where RR and VR are called the Rejection Ratio and the Volume Removal rate, respectively. In this paper, they are set as 1%. (6) Delete elements if < (th) ; (7) Repeat steps (1)(6) until either the maximum iteration number is reached or the solution is convergent. The total density change is calculated. The solution is considered to be convergent if the total mass is convergent (Weinans et al. 1992).

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2.3 Solution procedure The nite element analysis is implemented using ABAQUS. The following strategy is employed. In normal circumstance, a bone structure is in remodelling equilibrium and stress equilibrium. Changes either in the bone structure (e.g., caused during surgery) or in the external loads will break the remodelling equilibrium and then stimulate the remodelling process. The remodelling process can be divided into two steps. The rst step is of a short time period, in which the external load is set up and kept unchanged in the following process. As the rst step is short, there is almost no bone remodelling. The second much longer step involves bone remodelling, and material properties are updated according to the values of density. A solution-dependent state variable is used to save the density and another one controls the element deletion. The bone remodelling process is integrated in the User-subroutine UMAT, in which, the density is evaluated and saved into a solution-dependent state variable. The material properties vary depending on this solution-dependent state variable.

Fig. 1 Schematic illustration of trabeculae-like bone architecture observed in an animal experiment

3 Examples and results In order to validate the proposed methodology for external remodelling, two examples were analysed. 3.1 Bone remodelling between the bone a cylindrical implant interface When an implant is placed in a living bone tissue, the tissue remodels itself to accommodate the implant. The remodelling involves changes of the bone architecture in the vicinity of the implant. Bobyn et al. (1987) and Gross et al. (1990) reported that trabeculae-like spokes formed around the implant (as shown in Fig. 1). Luo et al. (1999) developed a numerical scheme which combined a surface remodelling theory and the boundary element method to study the formation of spokes in the vicinity of the implant. They represented the trabeculaelike bone architecture by a simplied model of spokes surrounding an implant (Fig. 2). They considered several models with different angles between two spokes. The simplest model is the one shown in Fig. 3, which corresponds to a right angle between two spokes. In this paper, we apply the topology optimisation technique to a model represented by Fig. 3 and simulate the bone remodelling process around the implant. The geometric parameters are: R = 1 mm, hx = hy = 2 mm, and wx = wy = 0.3 mm with uniform loads of 5N /mm2

Fig. 2 Simplied model of spokes surrounding an implant

applied across the widths of wx and wy vertically and horizontally. Figure 3 shows the mesh used, which consisted of 2,437 elements. The stimulus (= S/ ) is, as a rule, measured per element, indicating one sensor per element, and the density is also adapted per element. In the calculations, a uniform initial density distribution of = 0.8 g/cm3 is assumed. The starting density is that of a cancellous bone with about 55% porosity and 45% of the density of compact bone (which is 1.8 g/cm3 ). Poissons ratio is taken to be 0.3 and the reference signal value, k, is 0.07 J/g. The constant which relates the den2 sity and Youngs modulus, C, is 100 (MPa)/ g/cm3 and the remodelling rate B = 1.0 g/cm3 (Xinghua et al. 2005).
2

(MPa time unit)

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w x = 0.3

R=1

hx= 2
Fig. 3 A model for bone remodelling around an cylindrical implant under biaxial loading

Figure 4 demonstrates the variation of the bone density during the remodelling process. The textures illustrate the progressive change of bone by resorption and deposition. The white colour represents the minimum value (0.020 g/cm3 ) and the black the maximum (1.8 g/cm3 ). Figure 5 shows the contour plots of the von Mises stress, which corresponds to the time steps illustrated in Fig. 4. The white colour represents the minimum value (0.002 /Nmm2 ) and the black the maximum (12.000 N/mm2 ). Figure 6 demonstrates the SED variation during the remodelling process. Figures 4, 5, and 6 show that initially the bone structure has a uniform density distribution but a varying stress eld. The location with higher stress generally has higher strain energy which stimulates bone growth, whereas the location with lower stress leads to bone resorption. The bone is resorbed rst from the middle of the diagonal line, as this part has lowest energy level. The frontier of the resorption moves inwards as the remodelling progresses. Soon after this, the bone is also resorbed from the centre of the arch. After the middle part has been resorbed two spokes have formed.

and a height of h = 34 mm; the load is applied across a width of LP = 60 mm on the top and bottom surfaces of a vertebral body. The load distribution (a young person) is shown in Fig. 7a, with Psid = 3.5 N/mm2 (at both sides) and Pcen = 0.3 N/mm2 (at centre). The vertical load is 117.3 N. The nite element mesh is shown in Fig. 7b with 5,054 triangular elements. As in the earlier example, a uniform initial density distribution of = 0.8 g/cm3 is used. The reference signal value, k, is 0.2 J/g and Poissons ratio 0.3; the constant, which relates the density and Youngs modulus, C, is 100(MPa)/(g/cm3 )2 and the remodelling rate 2 B = 1.0 g/cm3 /(MPa time unit). The unit of time does not inuence the results, only the interpretation of the results. Figure 8 demonstrates the variation of the bone density during the remodelling process. The textures illustrate the progressive change of bone by resorption and deposition. The white colour represents the minimum value 0.020 g/cm3 and the black the maximum 1.5 g/cm3 . Figure 9 shows the contour plots of the von Mises stress corresponding to the time steps illustrated in Fig. 8. The white colour represents the minimum value 0.001 N/mm2 and the black the maximum 2.400 N/mm2 . Figure 10 demonstrates the SED variation during the remodelling process. Figures 8, 9, and 10 show that at the beginning, the bone structure has a uniform density distribution but a varying stress eld. Generally the location with higher stress has higher strain energy which stimulates bone growth, whereas the location with lower stress leads to bone resorption. The bone becomes thinner and then disappears from the middle of the sides, and the vertebral shape forms. Meanwhile, the bone distribution inside the body becomes localized and the distribution resembles columns which are connected to the top and bottom surface. The main difference between what is shown in Fig. 8 as the result of adaptive modelling in the vertebral centrum, and in reality, is that the up and down trabeculae have no connecting cross struts. That occurs because no shear force was used in the simulation. In reality, connecting cross struts can resist shear stress and avoid buckling.

hy= 2

w y = 0.3

4 Discussion 3.2 Simulation of a vertebral body The remodelling process of a vertebral body has been studied by Xinghua et al. (2005, 2002). Following Xinghua et al. (2005, 2002), the initial design domain is assumed to be rectangular with a width of L = 64 mm Biological structures, such as bones and trees, are natural and simple examples for shape optimisation as they change their contours to adapt to external loads. Based on the observation in nature (tree butts and branch joints), Mattheck (1990) developed the Biological

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Growth Method. It is hypothesized that the process of self-optimisation in these structures is carried out through the swelling or shrinking of the soft outermost layer of material. Since the pioneer work by Mattheck and Burkhardt (1990) was published, this idea has been developed into ESO (Xie and Steven 1993, 1994, 1997)

and applied into engineering design successfully (Xie et al. 2002, 2005). This article is trying to apply principles and methods of ESO back to the problems of adaptive bone remodelling. In this study, a topology optimisation methodology has been developed and applied to predict the external

Modelling external bone adaptation using evolutionary structural optimisation Fig. 6 SED variation during the remodelling process

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Fig. 7 Finite element model for vertebral body. (a) Design domain and loading condition; (b) Finite element mesh (5,054 triangular elements)

Lp = 0.060 m Psid Pcen

L = 0.064 m

(a)

(b)

shape of bone structure and the density distribution quantitatively. Both internal and external remodelling is implemented in a single algorithm [Eq. (1)]. The simplied two-dimensional models for the trabecular bone around a cylindrical implant and a vertebra were analysed. The results show that the topology optimisation methodology can successfully determine the external shape of bone structure and the bone density at each material point. Compared with the normal bone adaptation model (Weinans et al. 1992), the ESO algorithm continually checks for redundant elements and deletes them. As no stress analysis and material updates are required on the deleted elements, the ESO saves computational cost.

In the numerical calculation, the time scale is closely related to the remodelling rate. As the Eq. (1) is implemented using the Forward Euler method, the stability condition must be satised. The stability condition is studied in detail by Cowin et al. (1993) and Harrigan and Hamilton (1993). In this study, the time scale was small enough to guarantee numerical stability. This was checked using the criterion in Cowin et al. (1993). One of the limitations of this research is that the remodelling theory does not include material anisotropy. It is well-known that bone is an anisotropic material (Gjelsvik 1973). Folgado et al. (2004) proposed a structural optimisation model for bone remodelling in which trabecular bone was modelled as an orthotropic

282 Fig. 8 Variation of bone density during the remodelling process (vertebral bone)

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porous material with periodic microstructures. Their study, however, prescribed the bone shape and optimized the bone density; in the sense of structural optimisation, it represented parameter optimisation rather than topology optimisation. This study was limited to linear and elastic analysis. Element deletion in general will cause an abrupt change either in material properties (soft kill) or the structural geometry (hard kill), with an associated stress concentration. As a consequence, a ne mesh is required. With a ne mesh, at each iteration, only a few

elements are deleted in the low-stress region; and thus it will suppress the stress concentration to a very low level.

4.1 Bone remodelling between the bone and a cylindrical implant interface Figure 4 illustrates the remodelling process and the nal spoke topology are very similar to those reported in Luo et al. (1999). In Luo et al. (1999) the resorption only

Modelling external bone adaptation using evolutionary structural optimisation Fig. 10 SED variation during the remodelling process (vertebral bone)

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started from a diagonal edge until the spokes formed, while this study shows that resorption starts rst from the diagonal edge and then at the surface. The difference may arise from the differences in the numerical methods and the bone remodelling theories. Instead of a nite element method, Luo et al. (1999) used boundary element method. For bone remodelling, they used the strain rate as a remodelling stimulus, rather than the SED. In Luo et al. (1999), three different boundary conditions for the interface between the implant and the bone were studied: the xed, roller, and roller with gap, which describe the rough interface, smooth interface, and the smooth interface with a gap, respectively. They concluded that it was the gap instead of the roughness that inuenced the bone remodelling around the implant. Even though an accurate representation of a boundary condition is important, in this paper, the primary consideration is placed on the methodological issues and attention is limited to the roller boundary condition. 4.2 Simulation of the growth of vertebral body A vertebral body modies its external shape in the process of growth. Without an accurate prediction of the external shape, the process of vertebral body growth cannot be simulated adequately. In this simulation, the idea of topology optimisation was implemented, in which a design domain larger than the external shape of bone structure was used; the typical external shape of the

coronal section of a vertebral body was predicted instead of being chosen as the initial shape. Figure 8 shows that the predicted vertebral shape is much like the 2D used in Folgado et al. (2004) and Whyne et al. (2001). Folgado et al. (2004) presented a structural optimisation model to study bone remodelling for a human vertebra. Their study was limited to optimizing the bone density within an initially assumed design domain. Both a 2D and a 3D model were used and the material anisotropy was included. While the density distribution is similar to the remodelling results of a plate model (Weinans et al. 1992) with slanted loading, it is obviously different from the observation of Homminga et al. (2004), which was scanned with a CT scanner. The difference may be caused by an inaccuracy in loading conditions. Although a compressive force is undoubtedly the major component of the in vivo load, the actual load may consist of shear and torsional loads as well (Schultz et al. 1979; Tencer et al. 1982). Without considering shear and torsional loads, the results for the quarter of the vertebra model studied in this paper look very similar to the plate model studied by Weinans et al. (1992). Hence the bone distribution looks like many columns which are connected to the top and bottom surface. As the actual loading in a vertebra consists of shear and torsional loads, the scanned results (Homminga et al. 2004) show a stiffer horizontal linkage inside the vertebral body and this can resist shear stress. This study has shown that the ESO method has the potential to dene and predict the remodelling of bone

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G. Chen et al. Hassani B, Hinton E (1998) A review of homogenization and topology optimization Ihomogenization theory for media with periodic structure. Comput Struct 69(6):707717 Hegedus DH, Cowin SC (1976) Bone remodelling II: small strain adaptive elasticity. J Elast 6(4):337352 Hinton E (1998) Fully integrated design optimization.In: Steven GP, Querin OM, Guan H, Xie YM (eds) Proceedings of the Australasian Conference on structural optimisation. Oxbridge Press, Sydney, pp 329 Homminga J, Van-Rietbergen B, Lochmuller EM, Weinans H, Eckstein F, Huiskes R (2004) The osteoporotic vertebral structure is well adapted to the loads of daily life, but not to infrequent error loads. Bone 34(3):510516 Huiskes R, Weinans H, Grootenboer HJ, Dalstra M, Fudala, B., Slooff TJ (1987) Adaptive bone-remodeling theory applied to prosthetic-design analysis. J Biomech 20(1112): 11351150 Jacobs CR, Levenston ME, Beaupre GS, Simo JC, and Carter DR (1995) Numerical instabilities in bone remodeling simulations: the advantages of a node-based nite element approach. J Biomech 28(4):449459 Luo G, Sadegh AM, Alexander H, Jaffe W, Scott D, and Cowin SC (1999) The effect of surface roughness on the stress adaptation of trabecular architecture around a cylindrical implant. J Biomech 32(3):275284 Mattheck C (1990) Design and growth rules for biological structures and their application to engineering. Fatigue Fracture Eng Mater Struct 13(5):535550 Mattheck C, Burkhardt S (1990) A new method of structural shape optimization based on biological growth. Int J Fatigue 12(3):185190 Mattheck C, Tesari I (2003) The mechanical self-optimisation of trees. In: Proceedings of the Institute of Physics Conference, vol 180, pp 197206 Mattheck C, Burkhardt S, Erb D (1991) Shape optimization of engineering components by adaptive biological growth. In: Eschenauer H, Mattheck C, Olhoff N (eds) Engineering optimization in design processes, Springer, Berlin Heidelberg New York, pp 1524 Mullender MG, Huiskes R, Weinans H (1994) A physiological approach to the simulation of bone remodeling as a selforganizational control process. J Biomech 27(11):1389 1394 Mundy GR (1999) Bone remodeling and its disorders. Martin Dunitz, London Payten WM, Ben-Nissan B, Mercert DJ (1998) Optimal topology design using a global self-organisational approach. Int J Solids Struct 35(34):219237 Rice JC, Cowin SC, Bowman JA (1988) On the dependence of the elasticity and strength of cancellous bone on apparent density. J Biomech 21(2):155168 van Rietbergen B, Huiskes R, Weinans H, Sumner DR, Turner TM, Galante JO (1993) The mechanism of bone remodeling and resorption around press-tted THA stems. J Biomech 26(45):369382 Ruimerman R, Hilbers P, van Rietbergen B, Huiskes R (2005) A theoretical framework for strain-related trabecular bone maintenance and adaptation. J Biomech 38(4):931941 Schultz AB, Warwick DN, Berkson MH, Nachemson AL (1979) Mechanical properties of human lumbar spine motion segmentsPart 1. Responses in exion, extension, lateral bending, torsion. J Biomech Eng 101(1):4652 Tencer AF, Ahmed AM, Burke DL (1982) Some static mechanical properties of the lumbar intervertebral joint, intact and injured. J Biomech Eng 104(3):193201

in a particular stress eld. This will have applications in how to design scaffolds for articial bone substitute.

Acknowledgements This research was supported by a QUT Strategic Collaborative Program grant: Development of Bone Substitute Materials for Clinical Application.

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