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Αρχική σελίδα Ορθοπαιδικές Παθήσεις Βιογραφικό Έντυπο Συναίνεσης Ραντεβού Επικοινωνία - Τα 2 Ιατρεία

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MSc in Sports and Exercise Medicine, UCL

Physiology, Biochemistry and Nutrition module

Essay: “Discuss the role of tendons in athletic performance”

Konstantinos Bougoulias

CONTENTS:

    INTRODUCTION

    EMBRYOLOGY

    THE CELL BIOLOGY OF TENDON

    TENDON COLLAGEN

    NON-COLLAGENOUS MATRIX MACROMOLECULES OF TENDON

    BIOMECHANICAL EFFECTS OF EXERCISE

    SRUCTURAL EFFECTS OF EXERCISE

    SIGNIFICANCE OF ADAPTIVE CHANGES

    SUMMARY

    REFERENCES

Tendons are dense, well organized, fibrous constructs composed primarily of collagen fibrils that transmit the forces generated by muscle fibers to the skeletal system (Benjamin and Purslow) Their function is to transmit the force of muscle contraction, a function that requires a suite of integrated properties. How do they achieve these properties? The collagen fiber system is responsible for the bulk properties of the tissue. The organization of these fibers constrains the magnitude of overall deformation, and their strength and stiffness dominate the tensile mechanics. Extracellular matrix macromolecules contribute to the deformation properties of the tissue, and may play a significant role in mediating responses to dynamic loads and fatigue; but lets go into a detailed analysis of the issue starting from the very first beginning, the embryology.    

Embryology

Tendon arises from the lateral plate mesoderm, the same cells that give rise to endoskeletal cartilage. Though this tissue has biomedical significance there is very little research directed towards understanding the very early embryology of tendon.

We know a great deal more about both muscle and bone formation than we do about the tissue between them (D’Souza and Patel,1999). The involvment of TGFβ and scleraxis imly that there are similarities between pathways that pattern the skeleton and those at work in tendon, but particulars are far  from clear (Edom-Vovard et al,2002).

The cell biology of tendon

During growth and development tendon fibroblasts synthesize, assemble and construct complex extracellular supramolecular arrays with long range integrated architecture.The phenotypic expression of extracellular matrix macromolecules seems very likely to be under epigenetic control but the degree to which this plasticity is assimilated into the genome has not been explored. (Koob and Summers 2002).

Tendons attain an appropriate size and length in relation to muscle mass and distance from insertion during growth and development, therefore  tendon fibroblasts (tenocytes ) must continually monitor the magnitude and direction of load.The mechanism of load sensing remains a mystery; however, empirical work on isolated tendon fibroblasts has shown that they respond to mechanically indused strains (Banes and Banes 1999).White cells appear as separate , dispersed units in tendon ,they are in fact interconnected by extensive processes and gap junctions  and can communicate local conditions to neighboring cells (McNeilly et al. 1996)

Several distinct tissues, each with their own cell types, are associated with tendons: the tendon proper which consists of the collagen fascicles and inter-fascicular domains, a thin bounding layer of cells with little matrix called the epitenon ,and the sheath or peritenon.The development, properties and function of the cells that inhabit these tissues remains largely unexplored even in mammalian models (Koob 2002), and nothing is known about differentiated tendon cells in lower vertebrates.

Tendon collagen

Tendons are composed predominantly  of collagen organized into fibrils, fibers,fiber bundlels and fascicles, an organization presumed to be at the root of the mechanical properties of tendon. The fundamental unit is the type I collagen molecule, atriple helix composed of two α1 and one α2 chains.The α1  and α2 chains are products of different genes rather than post-tranlational modifications of a single molecule. Collagen molecules crystallize in specific linear arrays forming multi-molocular fibrillar aggregates easily visualized in electron micrographs as periodically banded fibrils.

Neighboring molecules are enzymatically polymerized after assembly in the extracellular matrix via lysine derived crosslinks. The extent and nature of crosslinking is variable, as pointed out by Shadwick et al (2002), but the taxonomic and functional variation is largely unexplored.

A commonly measured parameter of tendon collagen is fibril diameter, usually obtained from transmission electron micrographs. Fibrils vary in diameter as a function of age ,anatomical site and exercise. Tendons from young mammals have relatively small fibrils that fall within a unimodal distribution. As animals age,fibril diameters increase and generally segragate in biomodal distribution(Parry et al 1978).Dewin and Soslowsky (1999) also found a relationship between material properties  and fibril diameter.However, it is important to interpret these results with caution since there probably coincidental changes in the matrix. The causal mechanism of fibril diameter changes is likely rooted in changes  in the non-collagenous macromolecules of the matrix, and it is possible that material property changes have their basis here as well. In other words, until we have more information on the effects of fibril diameter and the extent of changes it is possible that it is an epiphenomenona of changes in the matrix.

The length and the shape of the collagen fibril are also important parameters to be measured. Impicit in reports of fibril diameter distributions from tendon is the assumption that fibrils are nearly uniform cylinders.If this assumption is correct, then a fibril’s measured diameter a valid descriptor ,and distributions indicate that cylindrical fibrils of varying diameter comprise tendon fibers.If instead the collagen fibrils have a spindle shape, as has been proposed by Trotter and Wofsy (1989), then diameter distribution is an artifact of sectioning different fibrils at different points along their tapering lengths. Surprisingly, after half a century of study on tendon fibril structure, the answer remains obscure, though the implications, functionally and organizationally, are important (Trotter, 2002)

A question related to the shape of the fiber, and no less difficult to address, is the issue of length. Do collagen fibrils span the entire tendon between the muscle and the point of insertion, or do fibrils end in the body of the tendon.This can be related to exercise adaptation and risk of rupture.There is little evidence to substantiate either hypothesis. However, Trotter and Wofsy (1989) reported that collagen fibrils in rat tail tendon taper and end within the body of the tendon. The answer to that question has immediate implications for the predominant mode of force transmission in tendon. Tendons are regarded as predominantly tensile structures, and if the fibrils are full length then they are certainly tensile structures. However, if the fibrils do not run the length of the tendon then force must be transmitted from one fibril to another. If the fibrils do not taper then tensile force can be transmitted through an abutting joint between fibrils, or through shear between adjacent fibrils. On the other hand , if the fibrils are tapering then the only possibility is that shear is the dominant mode of force transmission in the tendon. This would have implications for the natural mode of repair, the mechanics of failure, and the mechanism of fatigue.

Collagen concentration has been consistently measured in terms of  %  of dry weight. The majotity of existing studies do not support that collagen concentration changes due to exercise ( something that somebody would expect trying to explain possible biomechanical changes). Viidik (1967) did not find increased collagen concentration in the peroneous brevis tendons of trained rabbits, nor did Vailas et al. (1985) in the Achilles tendons of trained rats. Curwin et al. (1988) measured collagen concentration in the achilles tendon of growing chickens following an eight-week running program. Results indicated no difference in collagen concentration when compared to non-trained birds. Woo et al (1980) found that endurance training increased the collagen content of digital extensor tendons in swine, however, the same training regime had no effect on digital flexor tendons (Woo et al. 1981). They suggested that the different responses to exercise might be attributed to different biochemical composition. Compared to extensor tendons, the flexor tendons of control animals had lower contents of fat, water, and other non-collagenous proteins. Woo et al (1981 proposed that during exercise non-collagenous materials are diminished in extensor tendons, thus increasing the concentration of collagen and correspondingly changing the mechanical properties attributed to collagen. However, since the flexor tendons have already low amounts of non-collagenous materials, the concentration is not further reduced and hence changes in collagen concentration are not stimulated.

Studies addressing possible biochemical  alterations of tendon in response to long term training have focused on changes in collagen concentration. Current data suggest that training does not increase  collagen concentration (Viidik, 1967; Woo et al ,1980; Vailas et al., 1985;Curwin et al., 1988). Studies investigating the response of other biochemical variables to exercise are particularly sparse; therefore, it is impossible to make a definitive statement regarding the effect of exercise on these variables.  

Non-collagenous matrix macromolecules of tendon

In spite of their low relative abundance, non-collagenous extracellular macromolecules, either intimately associated with collagen fibrils or dispersed in the inter-fibrillar matrix or inter-fascicular domains, play important roles in tendon biology. There is not even a complete catalog of the molecules present in tendon from different vertebrates, let alone a clear idea of their function. However, empirical evidence suggests a role for at least a few of the more prevalent molecules.

Decorin, a dermatan sulphate-rich proteoglycan with a single glycosaminoglycan side chain, is so called because it “decorates” the assembled collagen fibrils in tendon. Decorin appears to wrap around the collagen at discrete locations, as a rudder band might hold together a sheath of pasta. Evidence from knock out mice and from in vitro collagen assembly experiments suggests that decorin in some way mediates the formation of collagen fibril. A controversial, but plausible hypothesis, is that it allows fibrils to increase in diameter up to a point and then prevents further self-assembly (Canty and Kadler, 2002) It is worth mentioning that in spite of clear morphological evidence that decorin spans collagen fibrils (Scott,2001), there is no experimental evidence at all, that they form cross links or have any effect on the material properties of tendon. This is an important area of research as the degree of cross linking has been imputed to affect stiffness (Buchanan and Buchanan).

Aggrecan, a very large proteoglycan, is found in high concentration in regions of tendon subjected to compressive loading. This molecule has a high fixed negative charge density and is responsible for much of the resilience in cartilage. Presumably it is playing a similar role here, though the mechanism of induction is not known. Other proteoglycans  including biglycan, fibromodulin, lumican and versican, are found in the tendon matrix, but essentially nothing is known about their function or their regulation. In addition to proteoglycans, tendon contains Type VI collagen in microfibrillar arrays, fibronectin associated with cells, and cartilage oligomeric matrix protein. Again, littke are known about the functional significance of these macromolecules, although they vary in abundance with respect to tendon type and regional specializations, age and exercise (Smith et al. 2002)

Vailas et al (1985) compared proteoglycan concentration in the Achilles tendons of adult sedentary rats to that of rats who had free access to a running wheel. They reported increased galactos-aminoglycan concentration in the exercising animals after six months, but not after 22 months. Curwin et al (1988) did not find significant changes in the galactosamine content of the Achilles tendon of exercised chicks. However, it is difficult to compare these results with those of Vailas et al. (1985), as immature tendon may respond to exercise differently than mature tendon.

Biomechanical effects of exercise

Studies that have examined mechanical changes of tendon in response to endurance training suggest that training results in increased tensile strength and stiffness (Table 1). This phenomenon has been reported for isolated free tendon (Viidik, 1967; Woo et al, 1980) as well as for the free tendon aponeurosis unit (Kubo et al., 2000; Buchanan and Marsh, 2001). Viidik (Viidik, 1967, 1969) studied adaptation of rabbit tibialis posterior, peroneal and  Achilles tendons to 40 weeks of training on a running machine. He reported an increase in stiffness of approximately 10% in the Achilles and tibialis posterior tendons; tensile strength of these tendons increased by approximately 5%. In studies of swine digital extensor tendons, Woo et al (1980), found that a twelve month training program that consisted of running at a maximal speed of 2.2 m/sec increased ultimate strength by 62%. The authors also noted increased stiffness of the extensor tendons. However, the same training regime had no effect on digital flexor tendons (Woo et al. , 1981). The authors noted that the digital flexors of swine work against large loads while the digital extensors seldom support large loads. The results of this study are perplexing in that changes did not occur in the tendons that were thought to be loaded during running.

Kiiskinen (1977) measured the failure strength of the patellar tendon of mice trained to run on a motorized treadmill. He reported that tensile strength of tendons from mice that trained for seven weeks did not differ significantly than that of control mice. However, Kiiskinen (1977) initiated training before the mice had completed growth, while VIIDIK (1967) and Woo et al (1980) trained adult animals. Also, Kiiskinen did not normalize data for cross-sectional area, as did the other two groups of investigators.

Vilarta and Vidal (1989) reported increased stiffness and tensile strength in the Achilles tendon of rats following a thirty day exercise program. Simonsen et al (1995) compared the adaptation response of Achilles tendon of rats to a strength training and a swimming (endurance) training regimen. No differences were reported in the force at ultimate tendon failure between 24-month-old or 29-month-old untrained and strength-trained groups. However, 29-month-old swin –trained rats showed tendons with average failure strength of 56.8N, which was significantly higher thn that (45.0 N)of untrained rats of the same age group. The authors did not measure tendon stiffness. These results are intriguing because they suggest that tendon properties may respond to the number of cycles of loading rather than load per sec.

Kubo et al. (2000) recently studied elastic properties of the tendon of the vastus lateralis in long-distance runners. They used ulrasonography to measure the stiffness of the combined free tendon and aponeurosis in vivo. The authors report a significant difference in stiffness of the vastus lateralis muscle of runners compared to control subjects.

The tendons of the runners was approximately 20% stiffer. In a more recent study, Kubo et al (2001) reported that isometric training also increased stiffness of the tendon structures of human knee extensor muscles. Buchanan and Marsh (2001) used sonomicrometry to measure stiffness of the free-tendon aponeurosis unit of the achilles tendon and lateral gastrocnemius muscle of guinea fowl. They reported increased stiffness in the combined tendons of birds that had exercised for twelve weeks on a motorized treadmill.

Although studies investigating the effects of long term training on tensile strength of tendon are limited, some patterns are beginning to emerge (Table 1). At least four studies report increased tensile strength in response to long term training (Viidik, 1967; Woo et al, 1980;Vilarta and Vidal, 1989; Simonsen et al, 1995). Three of these studies also report increased stiffness of at least one of the tendons studied (Vilarta and Vidal,1989; Viidik, 1967; Woo et al. 1980). This data suggest a correlation between increases in tendon strength and stiffness associated with long term training.

Structural effects of exercise

Increases in tendon stiffness and tensile strength reported following long term exercise could conceivably be attributed to tendon hypertrophy. However, current literature does not offer conclusive evidence to support this premise. In comparing the tendons of exercised rabbits to those of control animals, Viidik (1967) found no difference in either fresh weights or dry weights between groups. Similarly, Vailas et al. (1985) and Curwin et al (1988) found that training did not alter the dry weight of the patellar tendon of trained rats (Vailas) or the Achilles tendons of trained chicks (Curwin) Woo et al (1981) reported that long term training had no effect on the dry weight of the swine digital flexor tendons, however, increased dry weight of digital extensors. Kiiskinen (1977) reported that training indused a gain in the dry weight of Achilles tendons of growing mice, however, this phenomenon was not observed in adult mice. He suggested that the transient increase tendon weight during growth might be an indication of accelerated maturation.

A few studies have measured the cross sectional area of tendon following long term training.. Woo et al (1980) and Birch et al (19990 reported that the cross sectional area of digital extensor tendons of horses (Birch) and swine (Woo) increased in response to training. However, Birch et al (1999) pointed out that their subjects were still immature during training (2 years) and suggested that growth of the common digital extensor tendon was age related hypertrophy. Exercise had no effect on cross sectional area of the opposing flexor tendons in swine (Woo et al, 1981) or in horses. Buchnanan and Marsh (2001) found that the Achilles tendon of guinea fowl did not hypertrophy in response to long term training.

Inglemark (1948) compared collagen fibrils from the Achilles tendons of rats that had undergone approximately 40 weeks of daily running to those of untrained rats.He used electron microscopy to measure the thickness of fresh and OsO4-impegnated fibrils of trained animals were significantly thicker than those of untrained animals,this finding was not evident when comparing fresh collagen fibrils. More recently, Enwemeka et al (1992) studied the effect of exercise on the diameter of collagen fibrils taken from the Achilles tendons of rats. They reported an increase in collagen fibril diameter after ten weeks of exercise. However, Patterson-Kane et al (1998) reported that an 18-month treadmill-training program involving galloping did not change the mass-average diameter of collagen fibrils in the deep digital flexor tendon of horses.

A few investigations have focused on changes in the density and alignment of tendon collagen fibrils in response to exercise. Vilarta and Vidal (1989) observed more aligned and more intensely packed fibrils in the achilles tendons of rats after only thirty days of exercise. This team of investigators also noted increased tensile strength and stiffness in those tendons. In a study of the effect of exercise on the flexor digitorum longus tendon of mice, Michna and Hartmann(1989) reported an increase in collagen fibril number, however a decrease in fibril diameter aften ten weeks. Based on this limited and conflicting data, it is difficult to evaluate the effect of long term training on the size and or arrangement of collagen fibrils wthin tendon.

Significance of adaptive changes

Responsiveness of the musculoskeletal system to changes in use is generally thought to allow flexibility within the frame work of economical design. As opposed to the well documented changes in muscle with exercise (Wohl et al 2000), adaptive significance of changes in tendon with exercise is unclear. One possible reason  for changing stiffness would be to alter elastic energy storage. Elastic energy storage and subsequently release by tendons is hypothesized as a mechanism used to enhance economic locomotion (Alexander and Bennet-Clark, 1977; Taylor 1985;Roberts et al, 1997). However, the degree of tendon stiffness needed to maximize elastic energy storage is not known. Although under appropriate conditions increased tendon stiffness can provide the benefit of increased capacity to store elastic energy, it is doubtful that this is the impetus for tendon remodeling. By increasing stiffness the amount of energy stored can be substantially increased, but only if the force applied to the tendon substantially increases (fig.1). However, muscle forces do not increase during endurance type exercise. In comparing the cross sectional area of the lateral gastrocnemius muscle of exercised birds with that of control birds Buchanan and Marsh (2001) found no indication that the muscles of exercised birds had hypertrophied and would be better suited to exert higher forces. Futhermore, Kubo et al. (200) reported that increased tendon stiffness is not associated with increased elastic energy storage or muscle strength. These authors found significantly higher stiffness of the vastus lateralis tendon of long-distance runners compared to control subjects. However, during jumping movements, the same study revealed lower elastic energy storage potential in runners.

Another possible reason for tendon remodeling is to alter the ultimate failure strength of the tendon in response to increase loading. Increased tensile strength might be expected to maintain safety factors when the tendon is loaded. However, tendons may respond more readily to the number of cycles of loading than to the magnitude of the load. Simonsen et al (1995) found that a strength training regime (high force over a few loading cycles) did not stimulate increases in strength of the Achilles tendon of rats, however, low force endurance training in the form of swimming resulted in stronger tendons. These authors suggest that the tendons  may respond to the total number of muscle contractions  that occur during training rather than the absolute tension exerted by the muscle. Furthermore , the physiological loads that tendons normally bear are generally much less than failure strength. Carlstedt and Nordin (1989) noted that during normal activity, a tendon in vivo is subjected to less than 25% of its tensile strength.

Finally, increases in tendon stiffness observed following endurance training might not be associated with a requirement for increased strength, but rather represent a mechanism to resist tendon damage due to mechanical fatigue. This hypothesis is consistent with data reporting that endurance training in rats increased the tensile strength of tendons, but strength training did not (Simonsenet al., 1995). A tendon may be damaged by a single impact macro-trauma or from repetitive microtrauma. In testing the extensor digitorum longus tendon of the foot, Schechtman and Bader (1997) simulated an in vivo loading pattern. They found that when loaded at 20% of failure stress, tendon failure occurred at approximately 300 000 cycles, which is equivalent to approximately four months of normal walking. Fatigue occurring at this relatively low number of cycles makes it clear that repair and remodeling must continually occur in healthy tendons. For stabile function, the rate of repair must equal the rate of damage. Accumulated damage might occur if the number of load cycles increases. Decreased fatigability of a tendon may be an adaptive response that serves as a mechanism to prevent damage associated with repetitive loading.

Given the same load, increased stiffness will allow less extension of the tendon, which may result in less damage. This hypothesis may explain why Simonsen et al. (1995) found that tendons increased stiffness in response to a swim-training program even though this type of exercise has low impact loads. This conjecture may also explain why some tendons appear not to respond to exercise with changes in strength of stiffness. Pike et al. (2000) reported that while resistance to fatigue is higher in high-stressed tendons, no difference in stiffness was detected between high- and low-stressed tendons. This finding suggests that fatigability and stiffness may not always be correlated.

Summary

The majority of studies investigating tendon properties in response to exercise have been limited to measuring one or to variables (Buchanan, Marsh 2202). Further, few studies have integrated structural, biomechanical and biochemical parameters. This makes it difficult to definitively associate the mechanical properties of tendon with chemical composition and structure. Clearly, more research is needed before we can hope to understand what are the underlying mechanisms that result in stronger and/ or stiffer tendons  

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