Collagen Fiber Alignment and Maximum Principle Strain in the Axillary Pouch Predict Location of Failure During Uniaxial Extension

Author(s):  
Carrie A. Voycheck ◽  
Patrick J. McMahon ◽  
Richard E. Debski

The glenohumeral joint is frequently dislocated in the anterior direction causing injury to the anteroinferior (axillary pouch, anterior band of the inferior glenohumeral ligament (AB-IGHL)) capsule. [1, 2] When unloaded, the axillary pouch consists of randomly oriented collagen fibers. These fibers play a pertinent role in its function to resist loading in multiple directions during dislocation at the extreme ranges of motion. [3] Maximum principle strain directions in the anteroinferior capsule have been shown to align with the AB-IGHL during increasing external rotation, suggesting that the collagen fibers may become more aligned with loading as well. [4] In addition, at positions of increased external rotation, the peak maximum principle strains in the capsule correspond to the location of a common capsular failure known as the Bankart lesion. [4] Further, an increase in collagen fiber alignment with load in the supraspinatus tendon has been shown in the toe region of the load-elongation curve. [5] Therefore, it was hypothesized that increases in the collagen fiber alignment and maximum principle strain would correlate with the location of tissue failure. The objective of this work was to determine the collagen fiber alignment and maximum principle strain in the axillary pouch during uniaxial extension to failure and to determine if these parameters could predict the location of tissue failure.

Author(s):  
Kelvin Luu ◽  
Carrie A. Voycheck ◽  
Patrick J. McMahon ◽  
Richard E. Debski

The glenohumeral joint is frequently dislocated causing injury to the glenohumeral capsule (axillary pouch (AP), anterior band of the inferior glenohumeral ligament (AB-IGHL), posterior band of the inferior glenohumeral ligament (PB-IGHL), posterior (Post), and anterosuperior region (AS)). [1, 2] The capsule is a passive stabilizer to the glenohumeral joint and primarily functions to resist dislocation during extreme ranges of motion. [3] When unloaded, the capsule consists of randomly oriented collagen fibers, which play a pertinent role in its function to resist loading in multiple directions. [4] The location of failure in only the axillary pouch has been shown to correspond with the highest degree of collagen fiber orientation and maximum principle strain just prior to failure. [4, 5] However, several discrepancies were found when comparing the collagen fiber alignment between the AB-IGHL, AP, and PB-IGHL. [3,6,7] Therefore, the objective was to determine the collagen fiber alignment and maximum principal strain in five regions of the capsule during uniaxial extension to failure and to determine if these parameters could predict the location of tissue failure. Since the capsule functions as a continuous sheet, we hypothesized that maximum principal strain and peak collagen fiber alignment would correspond with the location of tissue failure in all regions of the glenohumeral capsule.


Author(s):  
Kristin S. Miller ◽  
Lena Edelstein ◽  
Louis J. Soslowsky

Cyclic preconditioning is a commonly accepted initial component of any tendon testing protocol. Preconditioning provides tendons with a consistent “history” and stress-strain results become repeatable allowing for rigorous evaluation and comparison. While it is widely accepted that preconditioning is important, changes that occur during preconditioning are not well understood. Micro-structural alterations, such as re-arrangement of collagen fibers, is one proposed mechanism of preconditioning [1,4]. However, this mechanism has not been examined. Therefore, the objective of this study is to locally measure: 1) fiber re-alignment during preconditioning, stress relaxation and tensile testing and 2) corresponding mechanical properties, to address mechanisms of preconditioning as well as tissue nonlinearity and inhomogeneity in the rat supraspinatus tendon. We hypothesize that 1) fiber re-alignment will be greatest in the toe region, but will also occur during preconditioning and 2) mechanical properties and initial collagen fiber alignment will be greater in the midsubstance location of the tendon compared to the tendon-to-bone insertion site.


Author(s):  
Kristin S. Miller ◽  
Brianne K. Connizzo ◽  
Elizabeth Feeney ◽  
Louis J. Soslowsky

One postulated mechanism of tendon structural response to mechanical load is collagen fiber re-alignment. Recently, where collagen fiber re-alignment occurs during a tensile mechanical test has been shown to vary by tendon age and location in a postnatal developmental mouse supraspinatus tendon (SST) model [1]. It is thought that as the tendon matures and its collagen fibril network, collagen cross-links and collagen-matrix interactions develop, its ability to respond quickly to mechanical stimuli hastens [1]. Additionally, the insertion site and midsubstance of postnatal SST may develop differently and at different rates, providing a potential explanation for differences in fiber re-alignment behaviors at the insertion site and midsubstance at postnatal developmental time points [1]. However, collagen fiber re-alignment behavior, in response to mechanical load at a mature age and in comparison to developmental ages, have not been examined. Therefore, the objectives of this study are to locally measure: 1) fiber re-alignment during preconditioning and tensile mechanical testing and 2) to compare local differences in collagen fiber alignment and corresponding mechanical properties to address tissue response to mechanical load in the mature and postnatal developmental mouse SST. We hypothesize that 1) 90 day tendons will demonstrate the largest shift in fiber re-alignment during preconditioning, but will also re-align during the toe- and linear-regions. Additionally, we hypothesize that 2) mechanical properties and initial collagen fiber alignment will be greater in the midsubstance of the tendon compared to the tendon-to-bone insertion site at 90 days, 3) that mechanical properties will increase with age, and that 4) collagen fiber organization at the insertion site will decrease with age.


Author(s):  
Carrie A. Rainis ◽  
Rouzbeh Amini ◽  
Richard E. Debski

Injury to the anteroinferior (anterior band of the inferior glenohumeral ligament (AB-IGHL) and axillary pouch) glenohumeral capsule is a common result of anterior dislocation [1]. Validated finite element models of the capsule can be used to address research questions regarding diagnostic and repair techniques targeted to this region of the capsule. However, these models require adequate constitutive models to describe capsule behavior. Structural models have improved predictions of capsule behavior compared to phenomenological models [2] but current experimental techniques used to measure fiber distributions in biologic soft tissues require that the sample be planar and cannot be performed on three-dimensional structures. Although recent work has demonstrated that the fiber kinematics in the capsule do not precisely follow the global tissue deformation [3], the affine assumption is presently the best approximation to provide initial insight into changes in collagen fiber alignment under moderate deformations. The collagen fibers in localized areas of planar samples from the anteroinferior capsule align with the direction of loading [4,5]; however, their behavior may be quite different during the complex loading conditions experienced by the intact capsule. Therefore, the objective of this work was to computationally project planar fiber distribution information to the three-dimensional glenohumeral capsule and use the affine assumption to quantify the change in fiber alignment of the anteroinferior glenohumeral capsule from an inflated reference state to three clinically relevant joint positions.


2021 ◽  
Author(s):  
Xingyu Chen ◽  
Dongning Chen ◽  
Ehsan Ban ◽  
Paul A. Janmey ◽  
Rebecca G. Wells ◽  
...  

AbstractCells can sense and respond to mechanical forces in fibrous extracellular matrices (ECM) over distances much greater than their size. This phenomenon, termed long-range force transmission, is enabled by the realignment (buckling) of collagen fibers along directions where the forces are tensile (compressive). However, whether other key structural components of the ECM, in particular glycosaminoglycans (GAGs), can affect the efficiency of cellular force transmission remains unclear. Here we developed a theoretical model of force transmission in collagen networks with interpenetrating GAGs, capturing the competition between tension-driven collagen-fiber alignment and the swelling pressure induced by GAGs. Using this model, we show that the swelling pressure provided by GAGs increases the stiffness of the collagen network by stretching the fibers in an isotropic manner. We found that the GAG-induced swelling pressure can help collagen fibers resist buckling as the cells exert contractile forces. This mechanism impedes the alignment of collagen fibers and decreases long-range cellular mechanical communication. We experimentally validated the theoretical predictions by comparing collagen fiber alignment between cellular spheroids cultured on collagen gels versus collagen-GAG co-gels. We found significantly less alignment of collagen in collagen-GAG co-gels, consistent with the prediction that GAGs can prevent collagen fiber alignment. The roles of GAGs in modulating force transmission uncovered in this work can be extended to understand pathological processes such as the formation of fibrotic scars and cancer metastasis, where cells communicate in the presence of abnormally high concentrations of GAGs.Statement of significanceGlycosaminoglycans (GAGs) are carbohydrates that are expressed ubiquitously in the human body and are among the key macromolecules that influence development, homeostasis, and pathology of native tissues. Abnormal accumulation of GAGs has been observed in metabolic disorders, solid tumors, and fibrotic tissues. Here we theoretically and experimentally show that tissue swelling caused by the highly polar nature of GAGs significantly affects the mechanical interactions between resident cells by altering the organization and alignment of the collagenous extracellular matrix. The roles of GAGs in modulating cellular force transmission revealed here can guide the design of biomaterial scaffolds in regenerative medicine and provides insights on the role of cell-cell communication in tumor progression and fibrosis.


Author(s):  
William J. Newman ◽  
Richard E. Debski ◽  
Susan M. Moore ◽  
Jeffrey A. Weiss

The shoulder is one of the most complex and often injured joints in the human body. The inferior glenohumeral ligament (IGHL), composed of the anterior band (AB), posterior band (PB) and the axillary pouch, has been shown to be an important contributor to anterior shoulder stability (Turkel, 1981). Injuries to the IGHL of the glenohumeral capsule are especially difficult to diagnose and treat effectively. The objective of this research was to develop a methodology for subject-specific finite element (FE) modeling of the ligamentous structures of the glenohumeral joint, specifically the IGHL, and to determine how changes in material properties affect predicted strains in the IGHL at 60° of external rotation. Using the techniques developed in this research, an improved understanding of the contribution of the IGHL to shoulder stability can be acquired.


2016 ◽  
Vol 21 (7) ◽  
pp. 071111 ◽  
Author(s):  
Dmitry D. Yakovlev ◽  
Marina E. Shvachkina ◽  
Maria M. Sherman ◽  
Andrey V. Spivak ◽  
Alexander B. Pravdin ◽  
...  

Author(s):  
Carrie A. Voycheck ◽  
Patrick J. McMahon ◽  
Richard E. Debski

Glenohumeral dislocation is a significant clinical problem and often results in injury to the anteroinferior (anterior band of the inferior glenohumeral ligament (AB-IGHL) and axillary pouch) glenohumeral capsule. [1] However, clinical exams to diagnose capsular injuries are not reliable [2] and poor patient outcome still exists following repair procedures. [3] Validated finite element models of the glenohumeral capsule may be able to improve diagnostic and repair techniques; however, improving the accuracy of these models requires adequate constitutive models to describe capsule behavior. The collagen fibers in the anteroinferior capsule are randomly oriented [4], thus the material behavior of the glenohumeral capsule has been described using isotropic models. [5,6] A structural model consisting of an isotropic matrix embedded with randomly aligned collagen fibers proved to better predict the complex capsule behavior than an isotropic phenomenological model [7] indicating that structural models may improve the accuracy of finite element models of the glenohumeral joint. Many structural models make the affine assumption (local fiber kinematics follow global tissue deformation) however an approach to account for non-affine fiber kinematics in structural models has been recently developed [8]. Evaluating the affine assumption for the capsule would aid in developing an adequate constitutive model. Therefore, the objective of this work was to assess the affine assumption of fiber kinematics in the anteroinferior glenohumeral capsule by comparing experimentally measured preferred fiber directions to the affine-predicted fiber directions.


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