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      Quantification of Internal Stress-Strain Fields in Human Tendon: Unraveling the Mechanisms that Underlie Regional Tendon Adaptations and Mal-Adaptations to Mechanical Loading and the Effectiveness of Therapeutic Eccentric Exercise

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          Abstract

          By virtue of their anatomical location between muscles and bones, tendons make it possible to transform contractile force to joint rotation and locomotion. However, tendons do not behave as rigid links, but exhibit viscoelastic tensile properties, thereby affecting the length and contractile force in the in-series muscle, but also storing and releasing elastic stain energy as some tendons are stretched and recoiled in a cyclic manner during locomotion. In the late 90s, advancements were made in the application of ultrasound scanning that allowed quantifying the tensile deformability and mechanical properties of human tendons in vivo. Since then, the main principles of the ultrasound-based method have been applied by numerous research groups throughout the world and showed that tendons increase their tensile stiffness in response to exercise training and chronic mechanical loading, in general, by increasing their size and improving their intrinsic material. It is often assumed that these changes occur homogenously, in the entire body of the tendon, but recent findings indicate that the adaptations may in fact take place in some but not all tendon regions. The present review focuses on these regional adaptability features and highlights two paradigms where they are particularly evident: (a) Chronic mechanical loading in healthy tendons, and (b) tendinopathy. In the former loading paradigm, local tendon adaptations indicate that certain regions may “see,” and therefore adapt to, increased levels of stress. In the latter paradigm, local pathological features indicate that certain tendon regions may be “stress-shielded” and degenerate over time. Eccentric exercise protocols have successfully been used in the management of tendinopathy, without much sound understanding of the mechanisms underpinning their effectiveness. For insertional tendinopathy, in particular, it is possible that the effectiveness of a loading/rehabilitation protocol depends on the topography of the stress created by the exercise and is not only reliant upon the type of muscle contraction performed. To better understand the micromechanical behavior and regional adaptability/mal-adaptability of tendon tissue it is important to estimate its internal stress-strain fields. Recent relevant advancements in numerical techniques related to tendon loading are discussed.

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          Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise.

          We hypothesized that an acute bout of strenuous, non-damaging exercise would increase rates of protein synthesis of collagen in tendon and skeletal muscle but these would be less than those of muscle myofibrillar and sarcoplasmic proteins. Two groups (n = 8 and 6) of healthy young men were studied over 72 h after 1 h of one-legged kicking exercise at 67% of maximum workload (W(max)). To label tissue proteins in muscle and tendon primed, constant infusions of [1-(13)C]leucine or [1-(13)C]valine and flooding doses of [(15)N] or [(13)C]proline were given intravenously, with estimation of labelling in target proteins by gas chromatography-mass spectrometry. Patellar tendon and quadriceps biopsies were taken in exercised and rested legs at 6, 24, 42 or 48 and 72 h after exercise. The fractional synthetic rates of all proteins were elevated at 6 h and rose rapidly to peak at 24 h post exercise (tendon collagen (0.077% h(-1)), muscle collagen (0.054% h(-1)), myofibrillar protein (0.121% h(-1)), and sarcoplasmic protein (0.134% h(-1))). The rates decreased toward basal values by 72 h although rates of tendon collagen and myofibrillar protein synthesis remained elevated. There was no tissue damage of muscle visible on histological evaluation. Neither tissue microdialysate nor serum concentrations of IGF-I and IGF binding proteins (IGFBP-3 and IGFBP-4) or procollagen type I N-terminal propeptide changed from resting values. Thus, there is a rapid increase in collagen synthesis after strenuous exercise in human tendon and muscle. The similar time course of changes of protein synthetic rates in different cell types supports the idea of coordinated musculotendinous adaptation.
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            Lack of tissue renewal in human adult Achilles tendon is revealed by nuclear bomb 14C

            Tendons are often injured and heal poorly. Whether this is caused by a slow tissue turnover is unknown, since existing data provide diverging estimates of tendon protein half-life that range from 2 mo to 200 yr. With the purpose of determining life-long turnover of human tendon tissue, we used the 14C bomb-pulse method. This method takes advantage of the dramatic increase in atmospheric levels of 14C, produced by nuclear bomb tests in 1955–1963, which is reflected in all living organisms. Levels of 14C were measured in 28 forensic samples of Achilles tendon core and 4 skeletal muscle samples (donor birth years 1945–1983) with accelerator mass spectrometry (AMS) and compared to known atmospheric levels to estimate tissue turnover. We found that Achilles tendon tissue retained levels of 14C corresponding to atmospheric levels several decades before tissue sampling, demonstrating a very limited tissue turnover. The tendon concentrations of 14C approximately reflected the atmospheric levels present during the first 17 yr of life, indicating that the tendon core is formed during height growth and is essentially not renewed thereafter. In contrast, 14C levels in muscle indicated continuous turnover. Our observation provides a fundamental premise for understanding tendon function and pathology, and likely explains the poor regenerative capacity of tendon tissue.—Heinemeier, K. M., Schjerling, P., Heinemeier, J., Magnusson, S. P., Kjaer, M. Lack of tissue renewal in human adult Achilles tendon is revealed by nuclear bomb 14C.
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              Region specific patellar tendon hypertrophy in humans following resistance training.

              To examine if cross-sectional area (CSA) differs along the length of the human patellar tendon (PT), and if there is PT hypertrophy in response to resistance training. Twelve healthy young men underwent baseline and post-training assessments. Maximal isometric knee extension strength (MVC) was determined unilaterally in both legs. PT CSA was measured at the proximal-, mid- and distal PT level and quadriceps muscle CSA was measured at mid-thigh level using magnetic resonance imaging. Mechanical properties of the patellar tendons were determined using ultrasonography. Subsequently, subjects performed 12 weeks of heavy resistance knee extension training with one leg (Heavy-leg), and light resistance knee extension training with the other leg (Light-leg). The MVC increased for heavy-leg (15 +/- 4%, P < 0.05), but not for light-leg (6 +/- 4%). Quadriceps CSA increased in heavy-legs (6 +/- 1%, P < 0.05) while unchanged in light-legs. Proximal PT CSA (104 +/- 4 mm(2)) was smaller than the mid-tendon CSA (118 +/- 3 mm(2)), which again was smaller than distal tendon CSA (127 +/- 2 mm(2), P < 0.05). Light-leg PT CSA increased by 7 +/- 3% (P < 0.05) at the proximal tendon level, but was otherwise unchanged. Heavy-leg PT CSA increased at the proximal and distal tendon levels by 6 +/- 3% and 4 +/- 2% respectively (P < 0.05), but was unchanged at the mid tendon level. PT stiffness increased in heavy-legs (P < 0.05) but was unchanged in light-legs. Modulus remained unchanged in both legs. To our knowledge, this study is the first to report tendon hypertrophy following resistance training. Further, the data show that the human PT CSA varies along the length of the tendon.
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                Author and article information

                Contributors
                Journal
                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                1664-042X
                28 February 2017
                2017
                : 8
                : 91
                Affiliations
                [1] 1School of Sport and Exercise Sciences, Liverpool John Moores University Liverpool, UK
                [2] 2Faculty of Health Sciences, Staffordshire University Stoke-on-Trent, UK
                [3] 3School of Healthcare Science, Manchester Metropolitan University Manchester, UK
                [4] 4Faculty of Medicine and Health Sciences, School of Medicine, University of Nottingham Derby, UK
                Author notes

                Edited by: Hans Hoppeler, University of Bern, Switzerland

                Reviewed by: Taija Finni, University of Jyväskylä, Finland; Sylvain Dorel, University of Nantes, France

                *Correspondence: Constantinos N. Maganaris c.maganaris@ 123456ljmu.ac.uk

                This article was submitted to Exercise Physiology, a section of the journal Frontiers in Physiology

                Article
                10.3389/fphys.2017.00091
                5328946
                28293194
                f0b2af22-7e16-407e-85b3-d1be46df7928
                Copyright © 2017 Maganaris, Chatzistergos, Reeves and Narici.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 23 September 2016
                : 02 February 2017
                Page count
                Figures: 3, Tables: 0, Equations: 0, References: 89, Pages: 11, Words: 9677
                Categories
                Physiology
                Review

                Anatomy & Physiology
                finite element modeling,tendon,eccentric exercise,tendinopathy,mechanical properties,plasticity

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