Three-dimensional topology optimization model to simulate the external shapes of bone

Elucidation of the mechanism by which the shape of bones is formed is essential for understanding vertebrate development. Bones support the body of vertebrates by withstanding external loads, such as those imposed by gravity and muscle tension. Many studies have reported that bone formation varies in response to external loads. An increased external load induces bone synthesis, whereas a decreased external load induces bone resorption. This relationship led to the hypothesis that bone shape adapts to external load. In fact, by simulating this relationship through topology optimization, the internal trabecular structure of bones can be successfully reproduced, thereby facilitating the study of bone diseases. In contrast, there have been few attempts to simulate the external structure of bones, which determines vertebrate morphology. However, the external shape of bones may be reproduced through topology optimization because cells of the same type form both the internal and external structures of bones. Here, we constructed a three-dimensional topology optimization model to attempt the reproduction of the external shape of teleost vertebrae. In teleosts, the internal structure of the vertebral bodies is invariable, exhibiting an hourglass shape, whereas the lateral structure supporting the internal structure differs among species. Based on the anatomical observations, we applied different external loads to the hourglass-shaped part. The simulations produced a variety of three-dimensional structures, some of which exhibited several structural features similar to those of actual teleost vertebrae. In addition, by adjusting the geometric parameters, such as the width of the hourglass shape, we reproduced the variation in the teleost vertebrae shapes. These results suggest that a simulation using topology optimization can successfully reproduce the external shapes of teleost vertebrae. By applying our topology optimization model to various bones of vertebrates, we can understand how the external shape of bones adapts to external loads.Author summary: In this paper, we developed a computational method to investigate the relationship between three-dimensional bone shape and external loads imposed on bones. Many studies report that bone formation varies in response to external loads. An increased external load induces bone synthesis, whereas a decreased external load induces bone resorption. This relationship led to the hypothesis that the shape of bones adapts to external load. However, it remains unclear whether this hypothesis can explain the shape of bones. Here, we constructed a three-dimensional mathematical model that imitates the cellular activities of bone formation to attempt the reproduction of the shape of teleost vertebrae. In teleosts, the shape of the vertebrae differs among the species. We set the multiple types of external load conditions in the simulations and compared the simulation results with different teleost vertebrae. The produced structures that can resist the deformation of the surrounding tissues exhibited multiple structural features similar to the vertebrae of several teleost species. This result shows that the formation of bone shape can be explained by the adaptation to external load.