| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
INVITED EDITORIALS
1Division of Molecular Physiology
Division of Mechanical Engineering and Mechatronics
University of Dundee
James Black Centre, Dow Street
Dundee, United Kingdom
Functional Molecular Biology Lab
Division of Molecular Physiology
University of Dundee
James Black Centre, Dow Street
Dundee, United Kingdom
e-mail: k.baar{at}dundee.ac.uk
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.
REFERENCES
This article has been cited by other articles:
|
|
 |
|
  D. Shin, T. Finni, S. Ahn, J. A. Hodgson, H.-D. Lee, V. R. Edgerton, and S. Sinha Effect of chronic unloading and rehabilitation on human Achilles tendon properties: a velocity-encoded phase-contrast MRI study J Appl Physiol, October 1, 2008; 105(4): 1179 - 1186. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
