Szczesny Spencer E, Peloquin John M, Cortes Daniel H, Kadlowec Jennifer A, Soslowsky Louis J, Elliott Dawn M
Department of Orthopaedic Surgery, University of Pennsylvania, Philadelphia, PA 19104, USA.
J Biomech Eng. 2012 Feb;134(2):021004. doi: 10.1115/1.4005852.
The heterogeneous composition and mechanical properties of the supraspinatus tendon offer an opportunity for studying the structure-function relationships of fibrous musculoskeletal connective tissues. Previous uniaxial testing has demonstrated a correlation between the collagen fiber angle distribution and tendon mechanics in response to tensile loading both parallel and transverse to the tendon longitudinal axis. However, the planar mechanics of the supraspinatus tendon may be more appropriately characterized through biaxial tensile testing, which avoids the limitation of nonphysiologic traction-free boundary conditions present during uniaxial testing. Combined with a structural constitutive model, biaxial testing can help identify the specific structural mechanisms underlying the tendon's two-dimensional mechanical behavior. Therefore, the objective of this study was to evaluate the contribution of collagen fiber organization to the planar tensile mechanics of the human supraspinatus tendon by fitting biaxial tensile data with a structural constitutive model that incorporates a sample-specific angular distribution of nonlinear fibers. Regional samples were tested under several biaxial boundary conditions while simultaneously measuring the collagen fiber orientations via polarized light imaging. The histograms of fiber angles were fit with a von Mises probability distribution and input into a hyperelastic constitutive model incorporating the contributions of the uncrimped fibers. Samples with a wide fiber angle distribution produced greater transverse stresses than more highly aligned samples. The structural model fit the longitudinal stresses well (median R(2) ≥ 0.96) and was validated by successfully predicting the stress response to a mechanical protocol not used for parameter estimation. The transverse stresses were fit less well with greater errors observed for less aligned samples. Sensitivity analyses and relatively affine fiber kinematics suggest that these errors are not due to inaccuracies in measuring the collagen fiber organization. More likely, additional strain energy terms representing fiber-fiber interactions are necessary to provide a closer approximation of the transverse stresses. Nevertheless, this approach demonstrated that the longitudinal tensile mechanics of the supraspinatus tendon are primarily dependent on the moduli, crimp, and angular distribution of its collagen fibers. These results add to the existing knowledge of structure-function relationships in fibrous musculoskeletal tissue, which is valuable for understanding the etiology of degenerative disease, developing effective tissue engineering design strategies, and predicting outcomes of tissue repair.
冈上肌腱的异质组成和力学性能为研究纤维性肌肉骨骼结缔组织的结构-功能关系提供了契机。以往的单轴测试表明，在平行和垂直于肌腱纵轴的拉伸载荷作用下，胶原纤维角度分布与肌腱力学性能之间存在相关性。然而，冈上肌腱的平面力学性能可能更适合通过双轴拉伸测试来表征，该测试避免了单轴测试中存在的非生理性无牵引边界条件的限制。结合结构本构模型，双轴测试有助于确定肌腱二维力学行为背后的具体结构机制。因此，本研究的目的是通过将双轴拉伸数据与包含非线性纤维样本特定角度分布的结构本构模型进行拟合，评估胶原纤维组织对人冈上肌腱平面拉伸力学性能的贡献。在几种双轴边界条件下对区域样本进行测试，同时通过偏振光成像测量胶原纤维方向。纤维角度直方图采用冯·米塞斯概率分布进行拟合，并输入到包含未卷曲纤维贡献的超弹性本构模型中。纤维角度分布较宽的样本比排列更整齐的样本产生更大的横向应力。该结构模型对纵向应力拟合良好（中位数R(2)≥0.96），并通过成功预测对未用于参数估计的力学方案的应力响应进行了验证。横向应力拟合效果较差，排列不整齐的样本误差更大。敏感性分析和相对仿射纤维运动学表明，这些误差并非由于胶原纤维组织测量不准确所致。更有可能的是，需要额外的代表纤维-纤维相互作用的应变能项来更接近地逼近横向应力。尽管如此，该方法表明冈上肌腱的纵向拉伸力学性能主要取决于其胶原纤维的模量、卷曲度和角度分布。这些结果增加了纤维性肌肉骨骼组织中结构-功能关系的现有知识，这对于理解退行性疾病的病因、制定有效的组织工程设计策略以及预测组织修复结果具有重要价值。
