Tendon mechanics: the argument heats up (2007)

INVITED EDITORIALSTendon mechanics: the argument heats upJennifer Z. Paxton, and Keith BaarJennifer Z. Paxton, and Keith BaarPublished Online:01 Aug 2007https://doi.org/10.1152/japplphysiol.00426.2007This is the final version - click for previous versionMoreSectionsPDF (35 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations tendon has long been undervalued. Most textbooks describe only one concept of this tissue: tendons attach muscles to bones. This is akin to saying that Michelangelo was a painter. Both statements are true but do not even begin to describe the importance of their subjects. In fact, tendons play an essential role in a number of physiological processes, including decreasing muscle injury (8), and, in humans, provided an evolutionary advantage for bipedal gait (3). Given this background, a deeper insight into tendon mechanics is long overdue.In attaching a compliant tissue to a stiff one, tendon has a very difficult mechanical role: overcoming impedance mismatch. Impedance mismatch occurs when two mechanically different tissues are joined, resulting in strain concentrations where injury is most likely to occur. Over the past year, tendon's role in decreasing impedance mismatch, and therefore strain concentrations and injury, has begun to be elucidated. The initial step was the discovery that tendon mechanics are not uniform; rather they have regional differences in stiffness along their length, ranging from compliant at the proximal (muscle) end to stiff at the distal (bone) end (2). Second, as suggested by Eliasson et al. (5) in this month's issue of the Journal of Applied Physiology, tendon viscoelasticity may serve to decrease any remaining strain concentrations. Interestingly, the same cellular mechanism may underlie both regional variability and viscoelasticity.Unlike steel, which, from a mechanical standpoint, is a purely elastic material, biological tissues are viscoelastic and therefore possess both elastic and viscous properties. This trait engenders several important mechanical consequences for tendons: 1) their mechanics are dependent on the rate at which they are strained, i.e., fast loading renders tendons stiffer with a higher capacity for energy storage than slow loading; 2) they lose a small amount of energy when they are strained, resulting in different stress-strain curves during loading and unloading (hysteresis); 3) the fluid within them reduces oscillations and shock by absorbing kinetic energy or dissipating it slowly (damping); and 4) if a tendon is held in a stretched position, the energy stored within the tendon will decrease over time (creep).The existing paradigm holds that a tendon's stiffness is dependent on the collagen fibers while the viscoelasticity relies on the ground substance. The ground substance of tendon contains proteoglycans, small proteins and glycosaminoglycans with a high water-binding capacity due to their negative charge. The current theory suggests that when a tendon is stretched, fluid is squeezed out, taking with it energy in the form of heat (6). During unloading, this loss of energy is seen as a decrease in the stress at any given strain. The work of Eliasson et al. (5) reported in this issue demonstrates that this traditionally accepted explanation is not sufficient. Eliasson and her colleagues (5) inactivate the plantar flexor muscles in rats using botulinum toxin and show that, in the absence of changes in either the water or the glycosaminoglycan content of the Achilles tendon, a decrease in its viscoelasticity occurs. This finding strongly indicates that another, yet-unknown factor within the tendon contributes significantly to tendon viscoelasticity.One likely candidate is heat, generated as a result of friction between collagen fibrils, fibers, and/or fascicles as they slide past one another during stretch. If the movement of the collagen molecules in relation to each other within the matrix was prevented during extension, a decrease in friction and therefore a decrease in viscoelasticity would be observed. One potential mechanism for stabilization of the collagen matrix could be an increase in cross-links between the collagen molecules. Increased cross-link density will restrict fibrillar sliding during deformation, resulting in less frictional energy lost. In addition, increased cross-link density would increase the stiffness of the tendon (9), a property also observed in the Achilles tendons studied by Eliasson et al. (5).Cross-linking of collagen can occur by two distinct methods; enzymatic cross-linking mediated by lysyl oxidase, and nonenzymatic or glycation cross-linking (11). Cross-linking is greater in the distal region of tendons (4) and may provide an explanation for the regional variations in tendon mechanics described earlier (2). The regional variation in cross-links may, in turn, have a mechanical explanation. At the myotendinous junction, multiple invaginations between the muscle and tendon serve not only to increase the surface area for attachment of the two tissues but act to ensure that the interface is loaded in shear, rather than in tension (12). Shear forces may mechanically break the cross-links between collagen molecules in the proximal region of the tendon, but as the shear force decreases along the length of the tendon, cross-links will begin to remain intact and the stiffness of the tendon will increase, resulting in the distribution observed by Curwin et al. (4). When a muscle is inactivated, shear forces may no longer disrupt cross-link formation within the proximal tendon, resulting in greater cross-linking, increased stiffness, and decreased viscoelasticity.This model fits with the studies by both Arruda et al. (2) and the current study by Eliasson et al. (5) but contradicts a number of earlier studies asserting that tendon stiffness decreases with inactivity (for example, Refs. 1, 10). The primary difference between these two camps is the technique by which tendon mechanics are determined. The ex vivo tests that have shown a decrease in stiffness use only the central portion of the tendon, severed from its bone and muscle connections, whereas the in vivo human studies use only one reference point for their measurements. Testing in this fashion may not sufficiently consider the regional variability of the tendon. Indeed, since it is now known that most of the mechanical changes with inactivity occur within the proximal region of the tendon (2), it seems clear that the whole tendon unit or multiple external markers should be used.The other major concern with the human studies is their reliance on muscle contraction to load the tendon. As described above, because of the viscoelastic nature of tendon, the loading rate must be identical between tests to provide reliable mechanical data. By definition, a slower muscle contraction produces less stiffness than a fast muscle contraction in the same tendon. The special challenge in loading tendon using muscle contraction is that the rate of contraction varies, decreasing following inactivity and increasing following exercise training (7). This suggests that the use of an external loading device is more likely to yield a truly accurate measure of tendon mechanics.Michelangelo was the master of reproducing the human form. Tendon is the master mechanical tissue. It uses regional variability and viscoelasticity to overcome impedance mismatch and prevent musculoskeletal injury. We are only just beginning to understand tendon mechanics and how they are affected by activity. Now, it is important to revisit the cellular processes that underlie these mechanics. Specifically, the potential role of cross-links in determining viscoelasticity and stiffness needs to be investigated, both in humans and ex vivo in whole tendon units. Since tendons play a key role in decreasing musculoskeletal injury, the cross-link may be a potential target for drug therapies to improve tendon viscoelasticity and function.REFERENCES1 Almeida-Silveira MI, Lambertz D, Perot C, Goubel F. Changes in stiffness induced by hindlimb suspension in rat Achilles tendon. Eur J Appl Physiol 81: 252–257, 2000.Crossref | PubMed | ISI | Google Scholar2 Arruda EM, Calve S, Dennis RG, Mundy K, Baar K. Regional variation of tibialis anterior tendon mechanics is lost following denervation. J Appl Physiol 101: 1113–1117, 2006.Link | ISI | Google Scholar3 Bramble DM, Lieberman DE. Endurance running and the evolution of Homo. Nature 432: 345–352, 2004.Crossref | PubMed | ISI | Google Scholar4 Curwin SL, Roy RR, Vailas AC. Regional and age variations in growing tendon. J Morphol 221: 309–320, 1994.Crossref | ISI | Google Scholar5 Eliasson P, Fahlgren A, Pasternak B, Aspenberg P. Unloaded rat Achilles tendons continue to grow, but lose viscoelasticity. J Appl Physiol In press; doi:10.1152/japplphysiol.01333.2006.Google Scholar6 Elliott DM, Robinson PS, Gimbel JA, Sarver JJ, Abboud JA, Iozzo RV, Soslowsky LJ. Effect of altered matrix proteins on quasilinear viscoelastic properties in transgenic mouse tail tendons. Ann Biomed Eng 31: 599–605, 2003.Crossref | PubMed | ISI | Google Scholar7 Maganaris CN, Narici MV, Reeves ND. In vivo human tendon mechanical properties: effect of resistance training in old age. J Musculoskelet Neuronal Interact 4: 204–208, 2004.Google Scholar8 McHugh MP, Connolly DA, Eston RG, Kremenic IJ, Nicholas SJ, Gleim GW. The role of passive muscle stiffness in symptoms of exercise-induced muscle damage. Am J Sports Med 27: 594–599, 1999.Crossref | PubMed | ISI | Google Scholar9 Reddy GK, Stehno-Bittel L, Enwemeka CS. Glycation-induced matrix stability in the rabbit Achilles tendon. Arch Biochem Biophys 399: 174–180., 2002.Crossref | PubMed | ISI | Google Scholar10 Reeves ND, Maganaris CN, Ferretti G, Narici MV. Influence of 90-day simulated microgravity on human tendon mechanical properties and the effect of resistive countermeasures. J Appl Physiol 98: 2278–2286, 2005.Link | ISI | Google Scholar11 Reiser KM. Influence of age and long-term dietary restriction on enzymatically mediated crosslinks and nonenzymatic glycation of collagen in mice. J Gerontol 49: B71–B79, 1994.Crossref | PubMed | Google Scholar12 Trotter JA, Eberhard S, Samora A. Structural domains of the muscle-tendon junction. 1. The internal lamina and the connecting domain. Anat Rec 207: 573–591, 1983.Crossref | Google Scholar Download PDF Previous Back to Top Next FiguresReferencesRelatedInformation Cited ByTropocollagen springs allow collagen fibrils to stretch elasticallyActa Biomaterialia, Vol. 142The Influence of Active Hamstring Stiffness on Markers of Isotonic Muscle Performance20 May 2021 | Sports, Vol. 9, No. 5Basic Muscle Physiology in Relation to Hamstring Injury and Repair22 March 2020Water-content related alterations in macro and micro scale tendon biomechanics27 May 2019 | Scientific Reports, Vol. 9, No. 1An Analysis of the Mechanical Properties of the Ponseti Method in Clubfoot TreatmentApplied Bionics and Biomechanics, Vol. 2019In Situ Polyphosphate Nanoparticle Formation in Hybrid Poly(vinyl alcohol)/Karaya Gum Hydrogels: A Porous Scaffold Inducing Infiltration of Mesenchymal Stem Cells13 November 2018 | Advanced Science, Vol. 6, No. 2Pathogenesis and management of tendinopathies in sports medicine6 February 2018 | Translational Sports Medicine, Vol. 1, No. 1PAPP-A affects tendon structure and mechanical propertiesJournal of Structural Biology, Vol. 192, No. 1Reliability and consistency of plantarflexor stretch-shortening cycle function using an adapted force sledge apparatus22 March 2013 | Physiological Measurement, Vol. 34, No. 4Microstructural stress relaxation mechanics in functionally different tendonsMedical Engineering & Physics, Vol. 35, No. 1The mechanical properties of tail tendon fascicles from lubricin knockout, wild type and heterozygous miceJournal of Structural Biology, Vol. 176, No. 1A comparison of the quasi-static mechanical and non-linear viscoelastic properties of the human semitendinosus and gracilis tendonsClinical Biomechanics, Vol. 25, No. 4In situ multi-level analysis of viscoelastic deformation mechanisms in tendon collagenJournal of Structural Biology, Vol. 169, No. 2Effect of chronic unloading and rehabilitation on human Achilles tendon properties: a velocity-encoded phase-contrast MRI studyDongsuk Shin, Taija Finni, Sinyeob Ahn, John A. Hodgson, Hae-Dong Lee, V. Reggie Edgerton, and Shantanu Sinha1 October 2008 | Journal of Applied Physiology, Vol. 105, No. 4In vivo estimation and repeatability of force-length relationship and stiffness of the human achilles tendon using phase contrast MRIJournal of Magnetic Resonance Imaging, Vol. 28, No. 4 More from this issue > Volume 103Issue 2August 2007Pages 423-424 Copyright & PermissionsCopyright © 2007 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.00426.2007PubMed17446408History Published online 1 August 2007 Published in print 1 August 2007 Metrics