Structure and collagen crimp patterns of functionally distinct equine tendons, revealed by quantitative polarised light microscopy (qPLM)

Spiesz, Ewa M.; Thorpe, Chavaunne T.; Thurner, Philipp J.; Screen, Hazel R. C.

doi:10.1016/j.actbio.2018.01.034

Cited by 38 publications

(43 citation statements)

References 67 publications

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“…We speculate that the increased crimp frequency in the FDL may be a result of lower strain in the toe region during image capture. This finding is corroborated by equine work which showed increased crimp angles in positional tendons compared to energy‐storing tendons, which we also observed, but only early in fatigue loading . Taken together, this further supports the notion that crimp morphology is unique to tendon anatomical location and age, and similarities may exist across species.…”

Section: Discussionsupporting

confidence: 87%

Tendon Biomechanics and Crimp Properties Following Fatigue Loading Are Influenced by Tendon Type and Age in Mice

Zuskov

Freedman

Gordon

et al. 2019

Journal Orthopaedic Research

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In tendon, type‐I collagen assembles together into fibrils, fibers, and fascicles that exhibit a wavy or crimped pattern that uncrimps with applied tensile loading. This structural property has been observed across multiple tendons throughout aging and may play an important role in tendon viscoelasticity, response to fatigue loading, healing, and development. Previous work has shown that crimp is permanently altered with the application of fatigue loading. This opens the possibility of evaluating tendon crimp as a clinical surrogate of tissue damage. The purpose of this study was to determine how fatigue loading in tendon affects crimp and mechanical properties throughout aging and between tendon types. Mouse patellar tendons (PT) and flexor digitorum longus (FDL) tendons were fatigue loaded while an integrated plane polariscope simultaneously assessed crimp properties at P150 and P570 days of age to model mature and aged tendon phenotypes (N = 10–11/group). Tendon type, fatigue loading, and aging were found to differentially affect tendon mechanical and crimp properties. FDL tendons had higher modulus and hysteresis, whereas the PT showed more laxity and toe region strain throughout aging. Crimp frequency was consistently higher in FDL compared with PT throughout fatigue loading, whereas the crimp amplitude was cycle dependent. This differential response based on tendon type and age further suggests that the FDL and the PT respond differently to fatigue loading and that this response is age‐dependent. Together, our findings suggest that the mechanical and structural effects of fatigue loading are specific to tendon type and age in mice. © 2019 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 38:36–42, 2020

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Section: Discussionsupporting

confidence: 87%

Tendon Biomechanics and Crimp Properties Following Fatigue Loading Are Influenced by Tendon Type and Age in Mice

Zuskov

Freedman

Gordon

et al. 2019

Journal Orthopaedic Research

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“…Future studies could also pursue other potentially useful imaging modalities that could inform soft tissue structure-function relationships. For example, reversed clarified tissues can be histologically prepared for quantitative polarised light microscopy (qPLM) to investigate the structural arrangement of collagen and other fibrous proteins [51][52][53]. Therefore, 3D visualisation, image registration and subsequent analyses utilising bimodal imaging would greatly improve evaluation of a wide range of pre-clinical connective tissue disease models, as well as clinical samples.…”

Section: Discussionmentioning

confidence: 99%

Bimodal Whole-Mount Imaging of Tendon Using Confocal Microscopy and X-ray Micro-Computed Tomography

et al. 2020

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Background: Three-dimensional imaging modalities for optically dense connective tissues such as tendons are limited and typically have a single imaging methodological endpoint. Here, we have developed a bimodal procedure utilising fluorescence-based confocal microscopy and x-ray micro-computed tomography for the imaging of adult tendons to visualise and analyse extracellular sub-structure and cellular composition in small and large animal species. Results: Using fluorescent immunolabelling and optical clearing, we visualised the expression of the novel crossspecies marker of tendon basement membrane, laminin-α4 in 3D throughout whole rat Achilles tendons and equine superficial digital flexor tendon 5 mm segments. This revealed a complex network of laminin-α4 within the tendon core that predominantly localises to the interfascicular matrix compartment. Furthermore, we implemented a chemical drying process capable of creating contrast densities enabling visualisation and quantification of both fascicular and interfascicular matrix volume and thickness by x-ray micro-computed tomography. We also demonstrated that both modalities can be combined using reverse clarification of fluorescently labelled tissues prior to chemical drying to enable bimodal imaging of a single sample. Conclusions: Whole-mount imaging of tendon allowed us to identify the presence of an extensive network of laminin-α4 within tendon, the complexity of which cannot be appreciated using traditional 2D imaging techniques. Creating contrast for x-ray micro-computed tomography imaging of tendon using chemical drying is not only simple and rapid, but also markedly improves on previously published methods. Combining these methods provides the ability to gain spatio-temporal information and quantify tendon substructures to elucidate the relationship between morphology and function.

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“…Elastin and other structural constituents of these samples will be analyzed later by biochemical and microscopical analyses for further clarification of this matter. For instance, quantitative polarized light microscopy (Spiesz et al, 2018) could reveal differences in the collagen crimp patterns.…”

Section: Discussionmentioning

confidence: 99%

Comparison of elastic, viscoelastic and failure tensile material properties of knee ligaments and patellar tendon

Ristaniemi

Stenroth

Mikkonen

et al. 2018

Journal of Biomechanics

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The knee ligaments and patellar tendon function in concert with each other and other joint tissues, and are adapted to their specific physiological function via geometry and material properties. However, it is not well known how the viscoelastic and quasi-static material properties compare between the ligaments. The purpose of this study was to characterize and compare these material properties between the knee ligaments and patellar tendon. Dumbbell-shaped tensile test samples were cut from bovine knee ligaments (ACL, LCL, MCL, PCL) and patellar tendon (PT) and subjected to tensile testing (n = 10 per ligament type). A sinusoidal loading test was performed at 8% strain with 0.5% strain amplitude using 0.1, 0.5 and 1 Hz frequencies. Subsequently, an ultimate tensile test was performed to investigate the stress-strain characteristics. At 0.1 Hz, the phase difference between stress and strain was higher in LCL compared with ACL, PCL and PT (p < 0.05), and at 0.5 Hz that was higher in LCL compared with all other ligaments and PT (p < 0.05). PT had the longest toe-region strain (p < 0.05 compared with PCL and MCL) and MCL had the highest linear and strain-dependent modulus, and toughness (p < 0.05 compared with ACL, LCL and PT). The results indicate that LCL is more viscous than other ligaments at low-frequency loads. MCL was the stiffest and toughest, and its modulus increased most steeply at the toe-region, possibly implying a greater amount of collagen. This study improves the knowledge about elastic, viscoelastic and failure properties of the knee ligaments and PT.

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Structure and collagen crimp patterns of functionally distinct equine tendons, revealed by quantitative polarised light microscopy (qPLM)

Abstract: Graphical abstract

Cited by 38 publications

References 67 publications

Tendon Biomechanics and Crimp Properties Following Fatigue Loading Are Influenced by Tendon Type and Age in Mice

Tendon Biomechanics and Crimp Properties Following Fatigue Loading Are Influenced by Tendon Type and Age in Mice

Bimodal Whole-Mount Imaging of Tendon Using Confocal Microscopy and X-ray Micro-Computed Tomography

Comparison of elastic, viscoelastic and failure tensile material properties of knee ligaments and patellar tendon

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