Tensile properties and fiber alignment of human supraspinatus tendon in the transverse direction demonstrate inhomogeneity, nonlinearity, and regional isotropy (original) (raw)
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Tendon exhibits nonlinear stress-strain behavior that may be partly due to movement of collagen fibers through the extracellular matrix. While a few techniques have been developed to evaluate the fiber architecture of other soft tissues, the organizational behavior of tendon under load has not been determined. The supraspinatus tendon (SST) of the rotator cuff is of particular interest for investigation due to its complex mechanical environment and corresponding inhomogeneity. In addition, SST injury occurs frequently with limited success in treatment strategies, illustrating the need for a better understanding of SST properties. Therefore, the objective of this study was to quantitatively evaluate the inhomogeneous tensile mechanical properties, fiber organization, and fiber realignment under load of human SST utilizing a novel polarized light technique. Fiber distributions were found to become more aligned under load, particularly during the low stiffness toe-region, suggesting that fiber realignment may be partly responsible for observed nonlinear behavior. Fiber alignment was found to correlate significantly with mechanical parameters, providing evidence for strong structure-function relationships in tendon. Human SST exhibits complex, inhomogeneous mechanical properties and fiber distributions, perhaps due to its complex loading environment. Surprisingly, histological grade of degeneration did not correlate with mechanical properties. ß
Collagen fiber re-alignment and uncrimping are two postulated mechanisms of tendon structural response to load. Recent studies have examined structural changes in response to mechanical testing in a postnatal development mouse supraspinatus tendon model (SST), however, those changes in the mature mouse have not been characterized. The objective of this study was to characterize collagen fiber re-alignment and crimp behavior throughout mechanical testing in a mature mouse SST. METHOD OF APPROACH: A tensile mechanical testing set-up integrated with a polarized light system was utilized for alignment and mechanical analysis. Local collagen fiber crimp frequency was quantified immediately following the designated loading protocol using a traditional tensile set up and a flash-freezing method. The effect of number of preconditioning cycles on collagen fiber re-alignment, crimp frequency and mechanical properties in midsubstance and insertion site locations were examined. RESULTS: Decreases in collagen fiber crimp frequency were identified at the toe-region of the mechanical test at both locations. The insertion site re-aligned throughout the entire test, while the midsubstance re-aligned during preconditioning and the test's linear-region. The insertion site demonstrated a more disorganized collagen fiber distribution, lower mechanical properties and a higher cross-sectional area compared to the midsubstance location. CONCLUSIONS: Local collagen fiber re-alignment, crimp behavior and mechanical properties were characterized in a mature mouse SST model. The insertion site and midsubstance respond differently to mechanical load and have different mechanisms of structural response. Additionally, results support that collagen fiber crimp is a physiologic phenomenon that may explain the mechanical test toe-region.
Journal of Biomechanics, 2006
The tendon to bone insertion serves the mechanical role of transferring loads from a relatively compliant tendon to a relatively rigid bone. The details of the mechanism of load transfer are of great importance, since current surgical procedures for tendon reattachment have high failure rates. We hypothesized that the microscopic structure of the insertion is optimized to minimize stress concentrations associated with this load transfer. To explore this, collagen fiber orientation distributions were measured in the supraspinatus tendons of rats. The angular deviation of fibers was fairly uniform across the insertion, and the mean angles of the local distributions deviated mildly from the tendon axis. To explore how these observed property distributions could influence load transfer, these distributions were used to derive material properties for an idealized two-dimensional mechanical model of an insertion. Comparison between stress concentrations in this idealized model and those in three comparison models suggests that the microstructure serves to (1) simultaneously reduce stress concentrations and material mass, and (2) shield the insertion's outward splay from the highest stresses.
Biaxial tensile testing and constitutive modeling of human supraspinatus tendon
Journal of biomechanical engineering, 2012
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 supr...
Inhomogeneous mechanical behavior of the human supraspinatus tendon under uniaxial loading
Journal of Orthopaedic Research, 2005
Disorders of the rotator cuff, particularly tears of the rotator cuff tendons, cause significant shoulder disability. Among numerous factors thought to be responsible for the initiation and progression of supraspinatus tears are those related to the tendon's biomechanical properties. We hypothesized that in supraspinatus tendons subjected to tensile loading a strain gradient (difference) exists between the articular and bursal tendon surfaces, that regional strain differences exist on each of these two tendon surfaces, and that tendon surface strains vary with glenohumeral abduction. To test these hypotheses, the intrinsic inhomogeneous deformational characteristics of the articular and bursal surfaces of eight intact human cadaveric supraspinatus tendons were studied at three glenohumeral abduction angles using a novel multiple strain measuring system which simultaneously recorded surface marker displacements on two opposing soft tissue surfaces. Under applied tensile loads, the articular surface exhibited greater strain at 22 degrees (7.4+/-2.6% vs. 1.3+/-0.7%, p=0.0002) and 63 degrees (6.4+/-1.6% vs. 2.7+/-1.2%, p=0.0001) whereas the bursal surface exhibited greater strain at 90 degrees (7.6+/-2.8% vs. 4.9+/-0.4%, p=0.013). At all abduction angles, insertion strains were higher than those of the mid-tendon and tendon-muscle junction regions. The existence of inhomogeneous surface strains in the intact supraspinatus tendon demonstrates that intratendinous shear occurs within the tendon. The higher strain on the articular side of the tendon, especially at the insertion region, suggests a propensity for tears to initiate in the articular tendinous zone.
Journal of Anatomy, 2014
Achilles tendinopathies display focal tissue thickening with pain and ultrasonography changes. Whilst complete rupture might be expected to induce changes in tissue organization and protein composition, little is known about the consequences of non-rupture-associated tendinopathies, especially with regards to changes in the content of collagen type I and III (the major collagens in tendon), and changes in tendon fibroblast (tenocyte) shape and organization of the extracellular matrix (ECM). To gain new insights, we took biopsies from the tendinopathic region and flanking healthy region of Achilles tendons of six individuals with clinically diagnosed tendinopathy who had no evidence of cholesterol, uric acid and amyloid accumulation. Biochemical analyses of collagen III/I ratio were performed on all six individuals, and electron microscope analysis using transmission electron microscopy and serial block face-scanning electron microscopy were made on two individuals. In the tendinopathic regions, compared with the flanking healthy tissue, we observed: (i) an increase in the ratio of collagen III : I proteins; (ii) buckling of the collagen fascicles in the ECM; (iii) buckling of tenocytes and their nuclei; and (iv) an increase in the ratio of small-diameter : large-diameter collagen fibrils. In summary, load-induced non-rupture tendinopathy in humans is associated with localized biochemical changes, a shift from large-to small-diameter fibrils, buckling of the tendon ECM, and buckling of the cells and their nuclei.
Specialization of tendon mechanical properties results from interfascicular differences
Journal of The Royal Society Interface, 2012
Tendons transfer force from muscle to bone. Specific tendons, including the equine superficial digital flexor tendon (SDFT), also store and return energy. For efficient function, energy-storing tendons need to be more extensible than positional tendons such as the common digital extensor tendon (CDET), and when testedin vitrohave a lower modulus and failure stress, but a higher failure strain. It is not known how differences in matrix organization contribute to distinct mechanical properties in functionally different tendons. We investigated the properties of whole tendons, tendon fascicles and the fascicular interface in the high-strain energy-storing SDFT and low-strain positional CDET. Fascicles failed at lower stresses and strains than tendons. The SDFT was more extensible than the CDET, but SDFT fascicles failed at lower strains than CDET fascicles, resulting in large differences between tendon and fascicle failure strain in the SDFT. At physiological loads, the stiffness at th...
Distributions of types I, II and III collagen by region in the human supraspinatus tendon
Connective Tissue Research, 2013
The mechanical properties of the human supraspinatus tendon (SST) are highly heterogeneous and may reflect an important adaptive response to its complex, multiaxial loading environment. However, these functional properties are associated with a location-dependent structure and composition that have not been fully elucidated. Therefore, the objective of this study was to determine the concentrations of types I, II and III collagen in six distinct regions of the SST and compare changes in collagen concentration across regions with local changes in mechanical properties. We hypothesized that type I collagen content would be high throughout the tendon, type II collagen would be restricted to regions of compressive loading and type III collagen content would be high in regions associated with damage. We further hypothesized that regions of high type III collagen content would correspond to regions with low tensile modulus and a low degree of collagen alignment. Although type III collagen content was not significantly higher in regions that are frequently damaged, all other hypotheses were supported by our results. In particular, type II collagen content was highest near the insertion while type III collagen was inversely correlated with tendon modulus and collagen alignment. The measured increase in type II collagen under the coracoacromial arch provides evidence of adaptation to compressive loading in the SST. Moreover, the structure-function relationship between type III collagen content and tendon mechanics established in this study demonstrates a mechanism for altered mechanical properties in pathological tendons and provides a guideline for identifying therapeutic targets and pathology-specific biomarkers.
Mechanical properties of human patellar tendon at the hierarchical levels of tendon and fibril
Journal of Applied Physiology, 2012
Tendons are strong hierarchical structures, but how tensile forces are transmitted between different levels remains incompletely understood. Collagen fibrils are thought to be primary determinants of whole tendon properties, and therefore we hypothesized that the whole human patellar tendon and its distinct collagen fibrils would display similar mechanical properties. Human patellar tendons (n ϭ 5) were mechanically tested in vivo by ultrasonography. Biopsies were obtained from each tendon, and individual collagen fibrils were dissected and tested mechanically by atomic force microscopy. The Young's modulus was 2.0 Ϯ 0.5 GPa, and the toe region reached 3.3 Ϯ 1.9% strain in whole patellar tendons. Based on dry cross-sectional area, the Young's modulus of isolated collagen fibrils was 2.8 Ϯ 0.3 GPa, and the toe region reached 0.86 Ϯ 0.08% strain. The measured fibril modulus was insufficient to account for the modulus of the tendon in vivo when fibril content in the tendon was accounted for. Thus, our original hypothesis was not supported, although the in vitro fibril modulus corresponded well with reported in vitro tendon values. This correspondence together with the fibril modulus not being greater than that of tendon supports that fibrillar rather than interfibrillar properties govern the subfailure tendon response, making the fibrillar level a meaningful target of intervention. The lower modulus found in vitro suggests a possible adverse effect of removing the tissue from its natural environment. In addition to the primary work comparing the two hierarchical levels, we also verified the existence of viscoelastic behavior in isolated human collagen fibrils. atomic force microscopy; collagen; fibril dimensions; modulus; toe region TENDON TISSUE PLAYS AN ESSENTIAL role in transmitting contractile forces to bone to generate movement and is therefore uniquely designed to resist sizeable loads (up to ϳ8 times body wt) during human locomotion (16, 22). However, despite this inherent quality, both overuse injuries and complete tendon ruptures occur. The precise mechanism(s) for tendon injuries remains unknown, but it is possible that there are one or more "weak links" in the tendon structure (36).