Capturing sclera anisotropy using direct collagen fiber models. Linking microstructure to macroscopic mechanical properties.

Fengting Ji, Mohammad R. Islam, Frederick Sebastian, Hannah Schilpp, Bingrui Wang, Yi Hua, Rouzbeh Amini, Ian A Sigal
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Abstract

Because of the crucial role of collagen fibers on soft tissue mechanics, there is great interest in techniques to incorporate them in computational models. Recently we introduced a direct fiber modeling approach for sclera based on representing the long interwoven fibers. Our method differs from the conventional continuum approach to modeling sclera that homogenizes the fibers and describes them as statistical distributions for each element. At large scale our method captured gross collagen fiber bundle architecture from histology and experimental intraocular pressure-induced deformations. At small scale, a direct fiber model of a sclera sample reproduced equi-biaxial experimental behavior from the literature. In this study our goal was a much more challenging task for the direct fiber modeling: to capture specimen-specific 3D fiber architecture and anisotropic mechanics of four sclera samples tested under equibiaxial and four non-equibiaxial loadings. Samples of sclera from three eyes were isolated and tested in five biaxial loadings following an approach previously reported. Using microstructural architecture from polarized light microscopy we then created specimen-specific direct fiber models. Model fiber orientations agreed well with the histological information (adjusted R2's>0.89). Through an inverse-fitting process we determined model characteristics, including specimen-specific fiber mechanical properties to match equibiaxial loading. Interestingly, the equibiaxial properties also reproduced all the non-equibiaxial behaviors. These results indicate that the direct fiber modeling method naturally accounted for tissue anisotropy within its fiber structure. Direct fiber modeling is therefore a promising approach to understand how macroscopic behavior arises from microstructure.
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利用直接胶原纤维模型捕捉巩膜各向异性。将微观结构与宏观机械性能联系起来。
由于胶原纤维对软组织力学的重要作用,人们对将其纳入计算模型的技术非常感兴趣。最近,我们推出了一种基于长纤维交织的巩膜直接纤维建模方法。我们的方法不同于传统的连续体巩膜建模方法,后者将纤维均匀化,并将其描述为每个元素的统计分布。在大尺度上,我们的方法从组织学和眼内压引起的变形实验中捕捉到了胶原纤维束的结构。在小范围内,巩膜样本的直接纤维模型再现了文献中的等轴实验行为。在这项研究中,我们的目标是为直接纤维建模完成一项更具挑战性的任务:捕捉四个巩膜样本在等轴和四个非等轴载荷测试下的特定标本三维纤维结构和各向异性力学。按照之前报道的方法,从三只眼睛中分离出巩膜样本并进行了五次双轴载荷测试。利用偏振光显微镜观察到的微观结构,我们创建了针对具体样本的直接纤维模型。模型纤维方向与组织学信息非常吻合(调整后的 R2 值为 0.89)。通过反拟合过程,我们确定了模型的特征,包括与等轴荷载相匹配的特定标本纤维机械性能。有趣的是,等轴特性也再现了所有非等轴行为。这些结果表明,直接纤维建模方法自然地考虑了纤维结构中的组织各向异性。因此,直接纤维建模是了解微观结构如何产生宏观行为的一种有前途的方法。
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