Comparing continuum and direct fiber models of soft tissues: An ocular biomechanics example reveals that continuum models may artificially disrupt the strains at both the tissue and fiber levels

IF 9.4 1区 医学 Q1 ENGINEERING, BIOMEDICAL Acta Biomaterialia Pub Date : 2024-12-01 DOI:10.1016/j.actbio.2024.10.019
Xuehuan He , Mohammad R. Islam , Fengting Ji , Bingrui Wang , Ian A. Sigal
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Abstract

Collagen fibers are the main load-bearing component of soft tissues but difficult to incorporate into models. Whilst simplified homogenization models suffice for some applications, a thorough mechanistic understanding requires accurate prediction of fiber behavior, including both detailed fiber-level strains and long-distance transmission. Our goal was to compare the performance of a continuum model of the optic nerve head (ONH) built using conventional techniques with a fiber model we recently introduced which explicitly incorporates the complex 3D organization and interaction of collagen fiber bundles [1]. To ensure a fair comparison, we constructed the continuum model with identical geometrical, structural, and boundary specifications as for the fiber model. We found that: 1) although both models accurately matched the intraocular pressure (IOP)-induced globally averaged displacement responses observed in experiments, they diverged significantly in their ability to replicate specific 3D tissue-level strain patterns. Notably, the fiber model faithfully replicated the experimentally observed depth-dependent variability of radial strain, the ring-like pattern of meridional strain, and the radial pattern of circumferential strain, whereas the continuum model failed to do so; 2) the continuum model disrupted the strain transmission along each fiber, a feature captured well by the fiber model. These results demonstrate limitations of the conventional continuum models that rely on homogenization and affine deformation assumptions, which render them incapable of capturing some complex tissue-level and fiber-level deformations. Our results show that the strengths of explicit fiber modeling help capture intricate ONH biomechanics. They potentially also help modeling other fibrous tissues.

Statement of significance

Understanding the mechanics of fibrous tissues is crucial for advancing knowledge of various diseases. This study uses the ONH as a test case to compare conventional continuum models with fiber models that explicitly account for the complex fiber structure. We found that the fiber model captured better the biomechanical behaviors at both the tissue level and the fiber level. The insights gained from this study demonstrate the significant potential of fiber models to advance our understanding of not only glaucoma pathophysiology but also other conditions involving fibrous soft tissues. This can contribute to the development of therapeutic strategies across a wide range of applications.

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比较软组织的连续模型和直接纤维模型:一个眼部生物力学实例表明,连续模型可能会人为地破坏组织和纤维层面的应变。
胶原纤维是软组织的主要承重成分,但很难将其纳入模型中。虽然简化的均质化模型在某些应用中已经足够,但要彻底了解机理,就必须准确预测纤维的行为,包括详细的纤维级应变和长距离传输。我们的目标是比较使用传统技术建立的视神经头(ONH)连续模型与我们最近推出的纤维模型的性能,后者明确包含了胶原纤维束复杂的三维组织和相互作用[1]。为确保公平比较,我们在构建连续体模型时采用了与纤维模型相同的几何、结构和边界规格。我们发现1)尽管两种模型都能准确匹配实验中观察到的眼内压(IOP)诱导的全局平均位移反应,但它们在复制特定三维组织级应变模式的能力上存在显著差异。值得注意的是,纤维模型忠实地复制了实验观察到的随深度变化的径向应变、环状的经向应变模式和径向的周向应变模式,而连续体模型则没有做到这一点;2)连续体模型破坏了沿每根纤维的应变传递,而纤维模型很好地捕捉到了这一特征。这些结果表明了传统连续体模型依赖于均质化和仿射变形假设的局限性,使其无法捕捉某些复杂的组织级和纤维级变形。我们的研究结果表明,显式纤维建模的优势有助于捕捉复杂的 ONH 生物力学。它们还可能有助于其他纤维组织的建模。意义说明:了解纤维组织的力学对增进对各种疾病的了解至关重要。本研究以 ONH 为测试案例,比较了传统连续模型和明确考虑复杂纤维结构的纤维模型。我们发现,纤维模型能更好地捕捉组织层面和纤维层面的生物力学行为。从这项研究中获得的启示表明,纤维模型具有巨大的潜力,不仅能促进我们对青光眼病理生理学的理解,还能促进我们对涉及纤维软组织的其他病症的理解。这将有助于开发应用广泛的治疗策略。
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来源期刊
Acta Biomaterialia
Acta Biomaterialia 工程技术-材料科学:生物材料
CiteScore
16.80
自引率
3.10%
发文量
776
审稿时长
30 days
期刊介绍: Acta Biomaterialia is a monthly peer-reviewed scientific journal published by Elsevier. The journal was established in January 2005. The editor-in-chief is W.R. Wagner (University of Pittsburgh). The journal covers research in biomaterials science, including the interrelationship of biomaterial structure and function from macroscale to nanoscale. Topical coverage includes biomedical and biocompatible materials.
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