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Evolution of the Achilles tendon: The athlete's Achilles heel?
The Foot 21 (2011) 193–197
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The Foot journal homepage: www.elsevier.com/locate/foot
Review
Evolution of the Achilles tendon: The athlete’s Achilles heel? S. Malvankar a , W.S. Khan b,∗ a b
University College London Medical School, Gower Street, London, WC1E 6BT, United Kingdom University College London Institute of Orthopaedics and Musculoskeletal Sciences, Royal National Orthopaedic Hospital, Stanmore, Middlesex, HA7 4LP, United Kingdom
a r t i c l e
i n f o
Article history: Received 8 August 2011 Accepted 11 August 2011 Keywords: Achilles tendon Evolution Bipedal locomotion Athlete Tendinopathy
a b s t r a c t The Achilles tendon is believed to have first developed two million years ago enabling humans to run twice as fast. However if the Achilles tendon is so important in terms of evolution, then why is this tendon so prone to injury – especially for those more active like athletes. The Achilles tendon had an integral role in evolving apes from a herbivorous diet to early humans who started hunting for food over longer distances, resulting in bipedal locomotion. Evolutionary advantages of the Achilles tendon includes it being the strongest tendon in the body, having an energy-saving mechanism for fast locomotion, allows humans to jump and run, and additionally is a spring and shock absorber during gait. Considering these benefits it is therefore not surprising that studies have shown athletes have thicker Achilles tendons than subjects who are less active. However, contradictory to these findings that show the importance of the Achilles tendon for athletes, it is well known that obtaining an Achilles tendon injury for an athlete can be career-altering. A disadvantage of the Achilles tendon is that the aetiology of its pathology is complicated. Achilles tendon ruptures are believed to be caused by overloading the tensed tendon, like during sports. However studies have also shown athlete Achilles tendon ruptures to have degenerative changes in the tendon. Other flaws of the Achilles tendon are its non-uniform vascularity and incomplete repair system which may suggest the Achilles tendon is on the edge of evolution. Research has shown that there is a genetic influence on the predisposition a person has towards Achilles tendon injuries. So if this tendon is here to stay in our anatomy, and it probably is due to the slow rate of evolution in humans, research in genetic modification could be used to decrease athletes’ predisposition to Achilles tendinopathy. © 2011 Elsevier Ltd. All rights reserved.
Contents 1. 2. 3. 4. 5. 6.
How the tendon has evolved . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The tendon in athletes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Why is the tendon the way it is? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Is it here to stay? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . How will it continue to evolve?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Charles Darwin’s “On the Origin of Species” publication provoked controversy in the scientific establishment, at a time when the field had strong ties with the Church of England [1]. Before the discovery of DNA, he presented his notion that humans had primate ancestry [1]. Since then his concept of the evolutionary relationship between humans and apes has been confirmed by the correlation in the basic chemical sequences of myoglobin and haemoglobin molecules [2]. One characteristic which is thought to have evolved from apes to
∗ Corresponding author. Tel.: +44 0 7791 025554; fax: +44 0 1707 655059. E-mail address: [email protected] (W.S. Khan). 0958-2592/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.foot.2011.08.004
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humans is bipedal locomotion; this is thought to have been possible because of the lengthening of the Achilles tendon. Although some apes are able to walk bipedally to a small extent, humans as a species took bipedal terrestrial locomotion the furthest [3]. Primatologist Bill Sellers from Manchester University claimed that humans first developed the Achilles tendon more than two million years ago, enabling them to run twice as fast as before [4]. This concept of the Achilles tendon facilitating fast locomotion in humans had also been previously acknowledged by Dennis Bramble and Daniel Lieberman who wrote in Nature, 2004, that it was the Achilles tendon and gluteus maximus that are the important units utilized during running [4]. However two million years on from the development of the tendon in humans, injury to the Achilles tendon
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is the third most common major tendon disruption after rotatorcuff and knee tendon injuries [5], with 75–85% of these Achilles tendon ruptures associated with athletic activities [6]. So paradoxically even though fossil records show that the Achilles tendon helps with fast locomotion, this physiological structure seems to be a hindrance to the most physically active. Considering Charles Darwin’s other notion “survival of the fittest”, if the Achilles tendon makes the fittest of human beings like athletes susceptible to injury, then does this tendon still have an evolutionary importance or is it on the edge of disappearing from our anatomy. 1. How the tendon has evolved The development of the Achilles tendon helped facilitate the evolution from apes with a herbivorous diet to early hominins which had an omnivorous diet [3]. The Achilles tendon is absent or short in apes, meaning that their calf muscles extend right down to their tarsal bones [7]. This gave early apes the ability to display arboreal locomotion which corresponded with their herbivorous diet [3]. However the previously abundant food supplies in their environment became sparser and seasonal and so in order to adapt to these lifestyle changes the anatomy of the apes evolved [3]. Through fossil records, it can be seen that this lifestyle change would have been sustained easier by bipedal locomotion [3]. Early hominins had longer Achilles tendons than apes [8]. Their feet in contrast to apes had greatly reduced digits, parallel metatarsals and a longitudinal arch which allowed shock absorption and weight distribution – specialized for bipedalism [7]. They also had a larger calcaneus tuberosity which acted as a lever arm for plantar flexion [7]. Early hominins lived in woodlands and dry grassland, where food supplies were seasonal [3]. By living in an environment where the supply of nutrition fluctuated, it would have favored hominins to adapt their diet to a wider range of food (becoming omnivores), and to search for food over longer distances [3]. Research shows that the human lineage was initiated first by bipedalism, which then led to an increase in brain size and tool use [3]. A study investigating a population of hominins – the Dmanisi – discovered an abundance of tools and signs of butchery found at their site of habitat (southern Caucasus), indicating that this population were active hunters. The researchers also showed that the hind limb of the Dmanisi was functionally similar to a human’s, supporting the hypothesis that hunting is linked to the improvement and development of walking [9]. It is evident from these findings that the Achilles tendon alone does not facilitate bipedal locomotion behavior, as the whole anatomy of the foot evolved as well. All the bones and muscles involved in bipedal locomotion – the femora, tibiae, vertebrae and pelvis all differ in comparison to a non-bipedal animal [4]. It is clear that the role of the Achilles tendon is not for bipedal locomotion but for fast locomotion in particular such as hunting, so surely this tendon is an evolutionary advantage for athletes.
cross-sectional areas than the control group when comparing their dominant ankles [11]. So it seems evident that there is a relationship between fast locomotion (exercise) and the physical structure of the Achilles tendon. Obviously there is no clarification of which the cause is and which the effect is. Exercising probably increases the cross-sectional area of the muscle fascicles in the triceps surae and this consequently gives a thicker Achilles tendon [12]. However maybe those born with a thicker Achilles tendon are better at sports and that is why athletes tend to have thicker Achilles tendons. If the later explanation is true then this would support that the Achilles tendon is an evolutionary benefit to human beings, especially athletes. In contradiction a thicker Achilles tendon in its prominent locality, makes athletes more susceptible to injuries than inactive subjects. So even if the Achilles tendon is evolutionarily important it has an evolutionary flaw. In order to understand the evolutionary importance of having an Achilles tendon and seeing how this structure is relevant today in sports, it is useful to look individually at the three muscles that merge together and insert into the calcaneus to compose the Achilles tendon [13]. These three muscles are the posterior calf muscles – the gastronemius, soleus and plantaris which are all powerful flexors [13]. The gastronemius makes the bulk of the calf. It is a powerful muscle giving propulsive force in human evolutionary features such as running, walking and jumping [14]. So this muscle is vital in sports and this is exemplified when you wear high heels which shorten the gastronemius, consequently making it hard to walk as the muscle cannot fulfill its function properly [14]. The soleus muscle is an important postural muscle containing a higher proportion of slow fibres [14]. It prevents the body falling forwards at the ankle joint when standing [14]. So the insertion of the soleus into the Achilles tendon is essential to attain the upright posture needed for bipedal locomotion. One study found that the soleus muscle in rats responds to exercise by increasing the number of capillaries infiltrating the muscle [15]. Rats that ran during 27 months, had a larger soleus than the inactive rats [15]. The observation that the soleus muscle increases in size during exercise probably indicates that this muscle is important during fast locomotion as it helps sustain good balance [15]. Maybe that is why the Achilles tendon such a prominent locality, so that when it is subjected to a force, goli receptors in the tendon can be stimulated in order to maintain the posture by the soleus during exercise. Sever’s disease is a common traction apophysitis injury experienced in young athletes aged between 9 and 12 years. This condition occurs when there is contraction of the gastronemius-soleus complex leading to pain and inflammation of the heel and limited dorsiflexion [16]. So overall the gastronemius and soleus supply the Achilles tendon with many important advantages such as jumping, running and upright posture however overexertion of these muscles can give injury to athletes.
3. Why is the tendon the way it is? 2. The tendon in athletes Some studies have observed that the Achilles tendons in athletes are much thicker than compared to the tendons in subjects who are less active [10]. Emerson et al. found using ultrasonography, that the thickness of the Achilles tendons in gymnasts was significantly higher in five of the six measures carried out than the control group [10]. Ying et al. compared the thickness and crosssectional area of the Achilles tendons belonging to subjects who frequently exercised (two hour exercise sessions carried out at least three days a week), with subjects who did not exercise much (both groups were taken from a asymptomatic Chinese population) [11]. The results found that the group of subjects who exercised had significantly thicker Achilles tendons, with significantly higher
The plantaris muscle has a long delicate tendon which is stretched during walking and running exactly like a length of elastic [13]. An advantage of the Achilles tendon is that it is an important elastic energy store [13]. The plantaris tendon is able to return over ninety percent of the energy stored in this way during walking and running [13]. This is an important mechanism for camels and kangaroos in their locomotion [13]. During gait, kinetic energy lost at one stage of a stride is stored temporarily as elastic strain energy and returned later in an elastic recoil [17]. At high speeds, humans seem to save in this way more than half the metabolic energy they would otherwise need for locomotion [17]. One study found that there was an increased percentage of red fibres in the plantaris of young guinea pigs after a month of exercising, indicating that
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exercise increased the plantaris’ mitochondrial density with training [18]. All the observations seen in the young trained guinea pigs such as the smaller fibre areas and higher volume of fibres in the plantaris, indicated that training appeared to enhance the capacity of the plantaris for oxidative metabolism, which is more energy saving than anaerobic metabolism [18]. So another evolutionary benefit of the Achilles tendon is that it has an energy-saving mechanism from the plantaris and research shows that this mechanism is enhanced with sports. Even though contributions from each component muscle of the triceps surae have been found to increase the function of the Achilles tendon, some believe it is the triceps surae which is the cause of Achilles tendinopathy (which affects many athletes). It is believed that the uneven shortening of the muscles and non-uniform tendon force this would theoretically result in intratendinous shear strain and therefore cause sliding between the planes of tissue layers parallel to the acting forces [19]. Subsequently this shear stress could cause inflammation of the peritenon [20]. This paper has established that the Achilles tendon alone does not facilitate bipedal locomotion however if there is a rupture in the tendon the patient does display abnormal gait, which is unsuitable for the fast locomotion needed in most physically demanding sports. The Achilles tendon is biologically important for fast movement because it is needed in order to lift the heel in the final stages of the stride [21]. If there is an Achilles tendon rupture or gastroleal weakness, abnormal gait can precipitate, as the patient has insufficient ability to push off the foot during the terminal stance phase [21]. So for athletes, having an intact Achilles tendon is extremely important because without it would be difficult to practice their sport. The concept of increasing the length of the Achilles tendon for the development of human bipedal locomotion from ape arboreal locomotion has been also used for treating chronic Achilles tendonitis [22]. Achilles tendonitis is a condition where there is irritation and inflammation of the tendon and is a common injury in recreational athletes [22]. One of the treatments for chronic cases of Achilles tendonitis is lengthening of the Achilles tendon [22]. Lengthening of the Achilles tendon may be performed through three 0.5 cm incisions but does require a period of casting [22]. So the Achilles tendon is evolutionary important because without it gait is seriously compromised, additionally medical treatment used to restore the tendon’s excellent mechanical properties is based on evolution (i.e. lengthening the Achilles tendon). For example Achilles lengthening is used to overcome the abnormal gait caused by equinus deformity of the ankle in patients with cerebral palsy [23]. However one of the complications of surgically lengthening the Achilles tendon is over-lengthening it, so that the triceps surae becomes weakened, making them unable to sufficiently restrain the forward movement of the tibia, when the centre of gravity moves in front of the ankle centre of rotation during gait [23]. Crouched gait leads to increased work, early fatigue and decreased stride length [23]. So there seems that there is a definite limit to how far lengthening of the Achilles tendon during the evolution of humans, would be beneficial for fast locomotion. So maybe in terms of length the Achilles tendon really is on the edge of evolution. On the other hand, how can the Achilles tendon’s future in evolution be under threat when it is the strongest tendon in the body? The Achilles tendon is extremely strong because of it is composed of collagen fibres which pass downwards spiralling through some ninety degrees, with medial fibres passing posterior [14]. This unusual structure is believed to be responsible for the tendon’s elastic properties [14]. These elastic properties mean that during stressful actions such as jumping the strain is taken up by the Achilles tendon which produces a recoil effect [14]. Another advantageous feature of the engineering of the Achilles tendon is that it acts as a shock absorber and spring during fast locomotion [4]. A common condition experienced by athletes is plantar fasci-
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itis where the deep connective tissue at the bottom of the calcaneus is inflamed [4,24]. One study found that shock treatment through the Achilles tendon treated the plantar fasciitis for 77% of the 225 patients that were followed up after one year [25].
4. Is it here to stay? The debate about the future existence of the Achilles tendon has been conjured due to its vulnerability to injury. It does not seem comprehensible that a multifunctional tendon which is vital in bipedal locomotion should be so prone to damage, and even more prone in physically active and fitter humans. One study found that athletes who obtain an Achilles tendon injury can be for them career altering. It found that out of all the national American football players who sustained an Achilles tendon injury 36% never returned back to the sport, and those who did return were never able to return to their pre-injury levels of play [6]. Another study found that out of eighteen Irish dancers, fourteen were found to have Achilles tendinopathy [26]. Achilles tendonitis is a pain located around the Achilles tendon, often experienced by young athletes and middle aged men [27]. Achilles tendonitis in athletes is caused by overexertion usually caused by rapid loading of the tensed tendon [6]. In middle aged men, degeneration of the tendon tends to occur before the tendon ruptures, and patients need to wear an equinus plaster for eight weeks or be sutured surgically [27]. Surprisingly tendon degeneration has also been found in athletes. Achilles tendon ruptures are common in athletes and are believed to be caused by overuse, however it has been understood that ruptures can be caused by pre-existing tendon degeneration [28]. Studies have seen degenerative changes in the rupture regions of the Achilles tendon [28]. An evolutionary disadvantage of the Achilles tendon is its vascularity. Studies show that there is a relative decrease in the frequency and total area of vessels in the mid-portion of the Achilles tendon [29]. This is a factor in the pathological condition Achilles tendinosis [29]. Overuse of the tendon such as in sports can also lead to trauma where the tendon can no longer heal itself, and leads to mechanical breakdown [29]. Healthy tendons are 95% composed of Collagen I fibres [29]. These fibres possess a strong helical architecture, and are arranged in a highly organised manner to give tensile strength [29]. Collagen III seems to be the major collagen synthesized in the healing tendon after rupture, however they do not exhibit the tensile strength that of Collagen I [29]. So during repair with more Collagen III being synthesized than Collagen I this suggests that pathology in the Achilles tendon is combated with an incomplete repair process. This is probably why re-rupture of the Achilles tendon after surgical treatment is a common complication [29]. Physicians overlook around 25% of Achilles tendon ruptures, and this neglect can lead to deleterious results because of the tendon’s insufficient repair system [30]. For example conservatively treated neglected Achilles tendon ruptures can develop stump necrosis and atrophy of the gastronemius-soleus muscle [30]. Achilles tendinosis for athletes is sometimes treated surgically, and this procedure is where the degenerative tissue is debrided [28]. So another evolutionary flaw of the Achilles tendon is that it is not always able to heal itself to its original mechanical strength without medical intervention. However even the medical advances used to treat the Achilles tendon is not always fully effective. Using immobilisation of the ankle to allow the tendon to heal, can have contradictory results such as collagen degeneration, disorganisation and adhesion formation giving a stiffer less flexible tendon [5]. Surgery is more likely to be used to treat athletes with Achilles tendon rupture as so to help them return to their sport quicker [6]. However one of the challenges of using a surgical procedure to treat Achilles
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tendon rupture is trying to restore the original resting tension of the tendon as this is hard to predict [6]. If the resting tension is not restored the force–tension relationship of the muscle tendon unit is disturbed and this decreases the functional strength of the triceps surae [6]. Other complications of surgically repairing Achilles tendon ruptures are wound complications, adhesions and altered sensation [6]. So maybe the Achilles tendon is on the edge of evolution as it cannot repair itself sufficiently and even medical advances cannot turn the Achilles tendon to its pre-injury condition.
5. How will it continue to evolve? If the Achilles tendon has more evolutionary flaws than advantages for fast bipedal locomotion, then maybe it has no more evolutionary potential to offer. As already discussed the Achilles tendon cannot keep getting longer in length, as this would be detrimental to bipedal locomotion. However maybe there is room for evolution to change the insertion site of the tendon or to bring another mechanism instead of the Achilles tendon in order to give efficient fast bipedal locomotion. Local tendons such as the plantaris, posterior tibial, peronis brevis and flexor digitorum longus can be used as transferred grafts in order to surgically mend Achilles tendon ruptures [30]. Maybe it is possible that one of these local tendons will eventually replace the Achilles tendon when it has reached its limit in an evolutionary sense. There are some signs of the Achilles tendon degenerating, as 7–20% of limbs are absent of the plantaris muscle, an important constituent muscle of the tendon [31]. So if the absent plantaris becomes more common among the human population, the Achilles tendon would lack its energysaving mechanism which would make walking and running more energy consuming. However other than for sports, the need for fast locomotion of humans is not as great as it used to be, which may mean that this energy saving mechanism in the Achilles tendon is no longer essential for human survival. So perhaps the Achilles tendon will degenerate further, until there is no longer a need for it. One example of a tendon that is disappearing from our anatomy is the palmaris longus. This tendon is absent in around 15% of people [32]. A study carried out on Asian subjects with and without palmaris longus’ found that there was no significant difference in their grip and pinch strengths [32]. Maybe this occurrence will be true for the Achilles tendon where its presence or absence will make no difference to bipedal locomotion in the due course of evolution. A single regulatory change in a gene that controls other genes can change how a gene network works, with dramatic consequences for the phenotype [33]. Homeobox genes encode proteins that bind and regulate the expression of DNA in multi-cellular organisms [33]. An example of homeobox gene is Ultrabithorax which regulates the development of the thorax segment in Drosophila by regulating pathways of at least thirty genes [34]. Mutations of the bithorax locus results in production of an extra set of wings [34]. This could occur in a human population if, for example environmental segregation occurs [34]. This would limit gene drift and would impose different selection pressures on the separated populations [34]. It would be possible that a homeobox gene that regulates the pathway of the gene controlling the embryological development of the Achilles tendon could be affected. This could then lead to a different phenotype (a double Achilles tendon, shorter/longer Achilles tendon, different insertion). If this new phenotype was less vulnerable to damage, then maybe these genes would be passed onto future generations and evolution of the Achilles tendon would continue on. Mokone et al. investigated whether there was a genetic predisposition to Achilles tendon pathology. They investigated 111 Caucasian subjects with Achilles tendon pathology and compared to 129 controls and were genotyped for variations in the COL5A1
gene [35]. The study concluded that COL5A1 BstUI restriction fragment length polymorphisms is associated with Achilles tendon pathology [35]. So it seems that genes do affect predisposition to Achilles tendinopathy. If the homeobox gene that regulates the COL5A1 BstUI was mutated, then may be this would lead to an Achilles tendon which is less prone to pathology. The TT genotype appears to be a protective against acute soft tissue ruptures. Three studies have suggested that rare TT genotypes of the functional sp1 binding site polymorphism with intron 1 of COL1A1 are associated with Achilles tendon rupture [36]. By understanding that there is a genetic influence on the predisposition for Achilles tendinopathy, maybe it is possible for genetic research to help athletes to be more resistant to Achilles tendon injuries [36]. 6. Conclusion In summary the Achilles tendon is here to stay in our anatomy. This is not only because of the evolutionary advantages its possesses such as facilitating fast bipedal locomotion, acting as a spring and shock absorber during gait, supplying an energy saving mechanism during movement and being the strongest tendon in the body. Another valid reason why this tendon will stay in our anatomy for many generations to come is because the rate of evolution in the human species is very slow [37]. Evolution is much slower in humans because they have out-competed other rivalry species like the Neanderthals and that humans themselves have altered the environment around them to their benefit [37]. Humans have exterminated big predators and natural selection is much slower in industrial populations that developing countries [37]. Factors that would affect human evolution would be viruses, artificial genetic modification or if humans altered the environment too much to their detriment [37]. So it seems that the Achilles tendon will be present in the human race for many generations to come. Therefore we should focus our efforts in carrying out research to help cope with its complicated pathology and improve the efficiency of its treatments. Future treatments could use genetic modification to prevent the predisposition to Achilles tendon pathology, and this could be special interest for the sporting fields. Aspenberg found that tendon repair can be stimulated by a single application of one of the several growth factors including PDGF, TGF-␣, IGF-1, VEGF and GDF-5,6,7, or by a thrombocite concentrate [38]. The response is dependent on the mechanical microenvironment, which is crucial for the repair process [38]. Hopefully in the future, medical knowledge will have advanced enough for us to overcome the evolutionary flaws of the Achilles tendon. Conflict of interest None. References [1] Montgomery S. Charles Darwin. http://www.christs.cam.ac.uk/darwin200/ pages/index.php?page id=c8; 2009. Christ’s College, Cambridge. 4-5-2011. [2] Hall BM. Science and evolution as science. In: Evolution principles and processes; 2010. [3] Hall BM. Human origins and evolution. In: Evolution principles and processes; 2010. [4] Kamrani K. The role of the Achilles tendon on the origins of bipedalism & human evolution. http://anthropology.net/2007/09/11/the-role-of-the2007. achilles-tendon-on-the-origins-of-bipedalism-human-evolution/; Anthropology.net. 4-5-2011. [5] Lesic A, Bumbasirevic M. Disorders of the Achilles tendon. Curr Orthop 2004;18(1):63–75. [6] Shirzad K, Hewitt JD, Kiesa C. Return to football after Achilles tendon rupture. http://www.lowerextremityreview.com/article/return-to-football-afterachilles-tendon-rupture; 2010. 4-5-2011.
S. Malvankar, W.S. Khan / The Foot 21 (2011) 193–197 [7] The University of Texas At Austin. Primate anatomy. http://uts.cc. utexas.edu/∼bramblet/ant301/seven.html#anchor1842003; 2004. 4-5-2011. [8] The University of Waikato. Human evolution. http://sci.waikato. ac.nz/evolution/HumanEvolution.shtml; 2004. 4-5-2011. [9] Pontzer H, Rolian C, Rightmire GP, Jashashvili T, Ponce de León MS, Lordkipanidze D, et al. Locomotor anatomy and biomechanics of the Dmanisi hominins. J Hum Evol 2010;58(6):492–504. [10] Emerson C, Morrissey D, Perry M, Jalan R. Ultrasonographically detected changes in Achilles tendons and self reported symptoms in elite gymnasts compared with controls – an observational study. Man Ther 2010;15(1):37–42. [11] Ying M, Yeung E, Li B, Li W, Lui M, Tsoi CW. Sonographic evaluation of the size of Achilles tendon: the effect of exercise and dominance of the ankle. Ultrasound Med Biol 2003;29(5):637–42. [12] West DWD, Burd NA, Staples AW, Phillips SM. Human exercise-mediated skeletal muscle hypertrophy is an intrinsic process. Int J Biochem Cell Biol 2010;42(9):1371–5. [13] Dean C, Pegington J. The leg, ankle and foot. Core anatomy forstudents The Limbs and Vertebral Column. W.B. Saunders; 1996. p142-144. [14] Palastanga N. Lower limb: muscles plantarflexing the ankle joint. Anatomy and human movement stucture and function; 1998. [15] Brown M, Ross TP, Holloszy JO. Effects of ageing and exercise on soleus and extensor digitorum longus muscles of female rats. Mech Ageing Dev 1992;63(1):69–77. [16] Adirim TA, Barouh A. Common orthopaedic injuries in young athletes. Curr Paediatr 2006;16(3):205–10. [17] Alexander RM. Elastic energy stores in running vertebrates. Integr Comp Biol 1984;24(1):85–94. [18] Faulkner JA, Maxwell LC, Brook DA, Lieberman DA. Adaptation of guinea pig plantaris muscle fibers to endurance training. Am J Physiol 1971;221(1):291–7. [19] Moller JB, Hansen P, Aagaard P, Svantesson U, Kjaer M, Magnusson PS. Differential displacement of the human soleus and medial gastrocnemius aponeuroses during isometric plantar flexor contractions in vivo. http://jap.physiology.org/content/97/5/1908.full; 2011. 4-5-2011. [20] Lintz F, Higgs A, Millett M, Barton T, Raghuvanshi M, Adams MA, et al. The role of Plantaris Longus in Achilles tendinopathy: a biomechanical study. Foot Ankle Surg, in press, corrected proof. [21] Ramachandran M. Gait, Basic orthopaedic sciences: the Stanmore guide; 2007. [22] Oster JA. Achilles tendonitis. http://thesportfactory.com/site/trainingnews/ achillestendonitis.shtml; 2005. 4-5-2011.
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[23] Dietz FR, Albright JC, Dolan L. Medium-term follow-up of Achilles tendon lengthening in the treatment of ankle equinus in cerebral palsy. Iowa Orthop J 2006;(26):27–32. [24] Richie D. Plantar fasciitis: treatment pearls. http://www.aapsm.org/ plantar fasciitis.html; 2004. 4-5-2011. [25] Chuckpaiwong B, Berkson EM, Theodore GH. Extracorporeal shock wave for chronic proximal plantar fasciitis: 225 patients with results and outcome predictors. J Foot Ankle Surg 2003;48(2):148–55. [26] Walls RJ, Brennan SA, Hodnett P, O’Byrne JM, Eustace SJ, Stephens MM. Overuse ankle injuries in professional Irish dancers. Foot Ankle Surg 2010;16(1): 45–9. [27] Rowley DI, Dent JA. Foot and ankle. The musculoskeletal system:Core topics in the new curriculum. Chapman & Hall Medical; 1997. p283-284. [28] Almekinders LC, Garrett WE, Wilson FC. Sports injuries. Curr Probl Surg 2000;37(5):321–83. [29] Hargrove R, McLean C. Achilles tendon pathology. DeOrio JK. http://emedicine.medscape.com/article/1235456-overview; 2009. Medscape. 10-5-2010. [30] Mendicino SS, Reed TS. Repair of neglected Achilles tendon ruptures with a triceps surae muscle tendon advancement. J Foot Ankle Surg 2001;35(1): 13–8. [31] Spina AA. The plantaris muscle: anatomy, injury, imaging, and treatment. J Can Chiropr Assoc 2007;51(3):158–65. [32] Sebastin SJ, Puhaindran ME, Lim AY, Lim IJ, Bee WH. The prevalence of absence of the palmaris longus – a study in a Chinese population and a review of the literature. J Hand Surg Br 2005;30(5):525–7. [33] MedicineNet.com. Homeobox gene definition. http://www.medterms. com/script/main/art.asp?articlekey=3773; 2007. [34] Hall BM. Animals as a branch of the tree of life. Evolution principles and processes; 2010. [35] Mokone GG, Schwellnus MP, Noakes TD, Collins M. The COL5A1 gene and Achilles tendon pathology. Scand J Med Sci Sports 2006;16(1):19–26. [36] Collins M, Posthumus M, Schwellnus MP. The COL1A1 gene and acute soft tissue ruptures. Br J Sports Med 2010;44(14):1063–4. [37] Palme J. The future of Homo sapiens. The future of human evolution. http://web4health.info/en/aux/homo-sapiens-future.html; 2010. [38] Aspenberg P. Stimulation of tendon repair: mechanical loading, GDFs and platelets. A mini-review. Int Orthop 2007;31(6):783–9.
Contents lists available at SciVerse ScienceDirect
The Foot journal homepage: www.elsevier.com/locate/foot
Review
Evolution of the Achilles tendon: The athlete’s Achilles heel? S. Malvankar a , W.S. Khan b,∗ a b
University College London Medical School, Gower Street, London, WC1E 6BT, United Kingdom University College London Institute of Orthopaedics and Musculoskeletal Sciences, Royal National Orthopaedic Hospital, Stanmore, Middlesex, HA7 4LP, United Kingdom
a r t i c l e
i n f o
Article history: Received 8 August 2011 Accepted 11 August 2011 Keywords: Achilles tendon Evolution Bipedal locomotion Athlete Tendinopathy
a b s t r a c t The Achilles tendon is believed to have first developed two million years ago enabling humans to run twice as fast. However if the Achilles tendon is so important in terms of evolution, then why is this tendon so prone to injury – especially for those more active like athletes. The Achilles tendon had an integral role in evolving apes from a herbivorous diet to early humans who started hunting for food over longer distances, resulting in bipedal locomotion. Evolutionary advantages of the Achilles tendon includes it being the strongest tendon in the body, having an energy-saving mechanism for fast locomotion, allows humans to jump and run, and additionally is a spring and shock absorber during gait. Considering these benefits it is therefore not surprising that studies have shown athletes have thicker Achilles tendons than subjects who are less active. However, contradictory to these findings that show the importance of the Achilles tendon for athletes, it is well known that obtaining an Achilles tendon injury for an athlete can be career-altering. A disadvantage of the Achilles tendon is that the aetiology of its pathology is complicated. Achilles tendon ruptures are believed to be caused by overloading the tensed tendon, like during sports. However studies have also shown athlete Achilles tendon ruptures to have degenerative changes in the tendon. Other flaws of the Achilles tendon are its non-uniform vascularity and incomplete repair system which may suggest the Achilles tendon is on the edge of evolution. Research has shown that there is a genetic influence on the predisposition a person has towards Achilles tendon injuries. So if this tendon is here to stay in our anatomy, and it probably is due to the slow rate of evolution in humans, research in genetic modification could be used to decrease athletes’ predisposition to Achilles tendinopathy. © 2011 Elsevier Ltd. All rights reserved.
Contents 1. 2. 3. 4. 5. 6.
How the tendon has evolved . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The tendon in athletes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Why is the tendon the way it is? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Is it here to stay? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . How will it continue to evolve?. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Charles Darwin’s “On the Origin of Species” publication provoked controversy in the scientific establishment, at a time when the field had strong ties with the Church of England [1]. Before the discovery of DNA, he presented his notion that humans had primate ancestry [1]. Since then his concept of the evolutionary relationship between humans and apes has been confirmed by the correlation in the basic chemical sequences of myoglobin and haemoglobin molecules [2]. One characteristic which is thought to have evolved from apes to
∗ Corresponding author. Tel.: +44 0 7791 025554; fax: +44 0 1707 655059. E-mail address: [email protected] (W.S. Khan). 0958-2592/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.foot.2011.08.004
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humans is bipedal locomotion; this is thought to have been possible because of the lengthening of the Achilles tendon. Although some apes are able to walk bipedally to a small extent, humans as a species took bipedal terrestrial locomotion the furthest [3]. Primatologist Bill Sellers from Manchester University claimed that humans first developed the Achilles tendon more than two million years ago, enabling them to run twice as fast as before [4]. This concept of the Achilles tendon facilitating fast locomotion in humans had also been previously acknowledged by Dennis Bramble and Daniel Lieberman who wrote in Nature, 2004, that it was the Achilles tendon and gluteus maximus that are the important units utilized during running [4]. However two million years on from the development of the tendon in humans, injury to the Achilles tendon
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is the third most common major tendon disruption after rotatorcuff and knee tendon injuries [5], with 75–85% of these Achilles tendon ruptures associated with athletic activities [6]. So paradoxically even though fossil records show that the Achilles tendon helps with fast locomotion, this physiological structure seems to be a hindrance to the most physically active. Considering Charles Darwin’s other notion “survival of the fittest”, if the Achilles tendon makes the fittest of human beings like athletes susceptible to injury, then does this tendon still have an evolutionary importance or is it on the edge of disappearing from our anatomy. 1. How the tendon has evolved The development of the Achilles tendon helped facilitate the evolution from apes with a herbivorous diet to early hominins which had an omnivorous diet [3]. The Achilles tendon is absent or short in apes, meaning that their calf muscles extend right down to their tarsal bones [7]. This gave early apes the ability to display arboreal locomotion which corresponded with their herbivorous diet [3]. However the previously abundant food supplies in their environment became sparser and seasonal and so in order to adapt to these lifestyle changes the anatomy of the apes evolved [3]. Through fossil records, it can be seen that this lifestyle change would have been sustained easier by bipedal locomotion [3]. Early hominins had longer Achilles tendons than apes [8]. Their feet in contrast to apes had greatly reduced digits, parallel metatarsals and a longitudinal arch which allowed shock absorption and weight distribution – specialized for bipedalism [7]. They also had a larger calcaneus tuberosity which acted as a lever arm for plantar flexion [7]. Early hominins lived in woodlands and dry grassland, where food supplies were seasonal [3]. By living in an environment where the supply of nutrition fluctuated, it would have favored hominins to adapt their diet to a wider range of food (becoming omnivores), and to search for food over longer distances [3]. Research shows that the human lineage was initiated first by bipedalism, which then led to an increase in brain size and tool use [3]. A study investigating a population of hominins – the Dmanisi – discovered an abundance of tools and signs of butchery found at their site of habitat (southern Caucasus), indicating that this population were active hunters. The researchers also showed that the hind limb of the Dmanisi was functionally similar to a human’s, supporting the hypothesis that hunting is linked to the improvement and development of walking [9]. It is evident from these findings that the Achilles tendon alone does not facilitate bipedal locomotion behavior, as the whole anatomy of the foot evolved as well. All the bones and muscles involved in bipedal locomotion – the femora, tibiae, vertebrae and pelvis all differ in comparison to a non-bipedal animal [4]. It is clear that the role of the Achilles tendon is not for bipedal locomotion but for fast locomotion in particular such as hunting, so surely this tendon is an evolutionary advantage for athletes.
cross-sectional areas than the control group when comparing their dominant ankles [11]. So it seems evident that there is a relationship between fast locomotion (exercise) and the physical structure of the Achilles tendon. Obviously there is no clarification of which the cause is and which the effect is. Exercising probably increases the cross-sectional area of the muscle fascicles in the triceps surae and this consequently gives a thicker Achilles tendon [12]. However maybe those born with a thicker Achilles tendon are better at sports and that is why athletes tend to have thicker Achilles tendons. If the later explanation is true then this would support that the Achilles tendon is an evolutionary benefit to human beings, especially athletes. In contradiction a thicker Achilles tendon in its prominent locality, makes athletes more susceptible to injuries than inactive subjects. So even if the Achilles tendon is evolutionarily important it has an evolutionary flaw. In order to understand the evolutionary importance of having an Achilles tendon and seeing how this structure is relevant today in sports, it is useful to look individually at the three muscles that merge together and insert into the calcaneus to compose the Achilles tendon [13]. These three muscles are the posterior calf muscles – the gastronemius, soleus and plantaris which are all powerful flexors [13]. The gastronemius makes the bulk of the calf. It is a powerful muscle giving propulsive force in human evolutionary features such as running, walking and jumping [14]. So this muscle is vital in sports and this is exemplified when you wear high heels which shorten the gastronemius, consequently making it hard to walk as the muscle cannot fulfill its function properly [14]. The soleus muscle is an important postural muscle containing a higher proportion of slow fibres [14]. It prevents the body falling forwards at the ankle joint when standing [14]. So the insertion of the soleus into the Achilles tendon is essential to attain the upright posture needed for bipedal locomotion. One study found that the soleus muscle in rats responds to exercise by increasing the number of capillaries infiltrating the muscle [15]. Rats that ran during 27 months, had a larger soleus than the inactive rats [15]. The observation that the soleus muscle increases in size during exercise probably indicates that this muscle is important during fast locomotion as it helps sustain good balance [15]. Maybe that is why the Achilles tendon such a prominent locality, so that when it is subjected to a force, goli receptors in the tendon can be stimulated in order to maintain the posture by the soleus during exercise. Sever’s disease is a common traction apophysitis injury experienced in young athletes aged between 9 and 12 years. This condition occurs when there is contraction of the gastronemius-soleus complex leading to pain and inflammation of the heel and limited dorsiflexion [16]. So overall the gastronemius and soleus supply the Achilles tendon with many important advantages such as jumping, running and upright posture however overexertion of these muscles can give injury to athletes.
3. Why is the tendon the way it is? 2. The tendon in athletes Some studies have observed that the Achilles tendons in athletes are much thicker than compared to the tendons in subjects who are less active [10]. Emerson et al. found using ultrasonography, that the thickness of the Achilles tendons in gymnasts was significantly higher in five of the six measures carried out than the control group [10]. Ying et al. compared the thickness and crosssectional area of the Achilles tendons belonging to subjects who frequently exercised (two hour exercise sessions carried out at least three days a week), with subjects who did not exercise much (both groups were taken from a asymptomatic Chinese population) [11]. The results found that the group of subjects who exercised had significantly thicker Achilles tendons, with significantly higher
The plantaris muscle has a long delicate tendon which is stretched during walking and running exactly like a length of elastic [13]. An advantage of the Achilles tendon is that it is an important elastic energy store [13]. The plantaris tendon is able to return over ninety percent of the energy stored in this way during walking and running [13]. This is an important mechanism for camels and kangaroos in their locomotion [13]. During gait, kinetic energy lost at one stage of a stride is stored temporarily as elastic strain energy and returned later in an elastic recoil [17]. At high speeds, humans seem to save in this way more than half the metabolic energy they would otherwise need for locomotion [17]. One study found that there was an increased percentage of red fibres in the plantaris of young guinea pigs after a month of exercising, indicating that
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exercise increased the plantaris’ mitochondrial density with training [18]. All the observations seen in the young trained guinea pigs such as the smaller fibre areas and higher volume of fibres in the plantaris, indicated that training appeared to enhance the capacity of the plantaris for oxidative metabolism, which is more energy saving than anaerobic metabolism [18]. So another evolutionary benefit of the Achilles tendon is that it has an energy-saving mechanism from the plantaris and research shows that this mechanism is enhanced with sports. Even though contributions from each component muscle of the triceps surae have been found to increase the function of the Achilles tendon, some believe it is the triceps surae which is the cause of Achilles tendinopathy (which affects many athletes). It is believed that the uneven shortening of the muscles and non-uniform tendon force this would theoretically result in intratendinous shear strain and therefore cause sliding between the planes of tissue layers parallel to the acting forces [19]. Subsequently this shear stress could cause inflammation of the peritenon [20]. This paper has established that the Achilles tendon alone does not facilitate bipedal locomotion however if there is a rupture in the tendon the patient does display abnormal gait, which is unsuitable for the fast locomotion needed in most physically demanding sports. The Achilles tendon is biologically important for fast movement because it is needed in order to lift the heel in the final stages of the stride [21]. If there is an Achilles tendon rupture or gastroleal weakness, abnormal gait can precipitate, as the patient has insufficient ability to push off the foot during the terminal stance phase [21]. So for athletes, having an intact Achilles tendon is extremely important because without it would be difficult to practice their sport. The concept of increasing the length of the Achilles tendon for the development of human bipedal locomotion from ape arboreal locomotion has been also used for treating chronic Achilles tendonitis [22]. Achilles tendonitis is a condition where there is irritation and inflammation of the tendon and is a common injury in recreational athletes [22]. One of the treatments for chronic cases of Achilles tendonitis is lengthening of the Achilles tendon [22]. Lengthening of the Achilles tendon may be performed through three 0.5 cm incisions but does require a period of casting [22]. So the Achilles tendon is evolutionary important because without it gait is seriously compromised, additionally medical treatment used to restore the tendon’s excellent mechanical properties is based on evolution (i.e. lengthening the Achilles tendon). For example Achilles lengthening is used to overcome the abnormal gait caused by equinus deformity of the ankle in patients with cerebral palsy [23]. However one of the complications of surgically lengthening the Achilles tendon is over-lengthening it, so that the triceps surae becomes weakened, making them unable to sufficiently restrain the forward movement of the tibia, when the centre of gravity moves in front of the ankle centre of rotation during gait [23]. Crouched gait leads to increased work, early fatigue and decreased stride length [23]. So there seems that there is a definite limit to how far lengthening of the Achilles tendon during the evolution of humans, would be beneficial for fast locomotion. So maybe in terms of length the Achilles tendon really is on the edge of evolution. On the other hand, how can the Achilles tendon’s future in evolution be under threat when it is the strongest tendon in the body? The Achilles tendon is extremely strong because of it is composed of collagen fibres which pass downwards spiralling through some ninety degrees, with medial fibres passing posterior [14]. This unusual structure is believed to be responsible for the tendon’s elastic properties [14]. These elastic properties mean that during stressful actions such as jumping the strain is taken up by the Achilles tendon which produces a recoil effect [14]. Another advantageous feature of the engineering of the Achilles tendon is that it acts as a shock absorber and spring during fast locomotion [4]. A common condition experienced by athletes is plantar fasci-
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itis where the deep connective tissue at the bottom of the calcaneus is inflamed [4,24]. One study found that shock treatment through the Achilles tendon treated the plantar fasciitis for 77% of the 225 patients that were followed up after one year [25].
4. Is it here to stay? The debate about the future existence of the Achilles tendon has been conjured due to its vulnerability to injury. It does not seem comprehensible that a multifunctional tendon which is vital in bipedal locomotion should be so prone to damage, and even more prone in physically active and fitter humans. One study found that athletes who obtain an Achilles tendon injury can be for them career altering. It found that out of all the national American football players who sustained an Achilles tendon injury 36% never returned back to the sport, and those who did return were never able to return to their pre-injury levels of play [6]. Another study found that out of eighteen Irish dancers, fourteen were found to have Achilles tendinopathy [26]. Achilles tendonitis is a pain located around the Achilles tendon, often experienced by young athletes and middle aged men [27]. Achilles tendonitis in athletes is caused by overexertion usually caused by rapid loading of the tensed tendon [6]. In middle aged men, degeneration of the tendon tends to occur before the tendon ruptures, and patients need to wear an equinus plaster for eight weeks or be sutured surgically [27]. Surprisingly tendon degeneration has also been found in athletes. Achilles tendon ruptures are common in athletes and are believed to be caused by overuse, however it has been understood that ruptures can be caused by pre-existing tendon degeneration [28]. Studies have seen degenerative changes in the rupture regions of the Achilles tendon [28]. An evolutionary disadvantage of the Achilles tendon is its vascularity. Studies show that there is a relative decrease in the frequency and total area of vessels in the mid-portion of the Achilles tendon [29]. This is a factor in the pathological condition Achilles tendinosis [29]. Overuse of the tendon such as in sports can also lead to trauma where the tendon can no longer heal itself, and leads to mechanical breakdown [29]. Healthy tendons are 95% composed of Collagen I fibres [29]. These fibres possess a strong helical architecture, and are arranged in a highly organised manner to give tensile strength [29]. Collagen III seems to be the major collagen synthesized in the healing tendon after rupture, however they do not exhibit the tensile strength that of Collagen I [29]. So during repair with more Collagen III being synthesized than Collagen I this suggests that pathology in the Achilles tendon is combated with an incomplete repair process. This is probably why re-rupture of the Achilles tendon after surgical treatment is a common complication [29]. Physicians overlook around 25% of Achilles tendon ruptures, and this neglect can lead to deleterious results because of the tendon’s insufficient repair system [30]. For example conservatively treated neglected Achilles tendon ruptures can develop stump necrosis and atrophy of the gastronemius-soleus muscle [30]. Achilles tendinosis for athletes is sometimes treated surgically, and this procedure is where the degenerative tissue is debrided [28]. So another evolutionary flaw of the Achilles tendon is that it is not always able to heal itself to its original mechanical strength without medical intervention. However even the medical advances used to treat the Achilles tendon is not always fully effective. Using immobilisation of the ankle to allow the tendon to heal, can have contradictory results such as collagen degeneration, disorganisation and adhesion formation giving a stiffer less flexible tendon [5]. Surgery is more likely to be used to treat athletes with Achilles tendon rupture as so to help them return to their sport quicker [6]. However one of the challenges of using a surgical procedure to treat Achilles
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tendon rupture is trying to restore the original resting tension of the tendon as this is hard to predict [6]. If the resting tension is not restored the force–tension relationship of the muscle tendon unit is disturbed and this decreases the functional strength of the triceps surae [6]. Other complications of surgically repairing Achilles tendon ruptures are wound complications, adhesions and altered sensation [6]. So maybe the Achilles tendon is on the edge of evolution as it cannot repair itself sufficiently and even medical advances cannot turn the Achilles tendon to its pre-injury condition.
5. How will it continue to evolve? If the Achilles tendon has more evolutionary flaws than advantages for fast bipedal locomotion, then maybe it has no more evolutionary potential to offer. As already discussed the Achilles tendon cannot keep getting longer in length, as this would be detrimental to bipedal locomotion. However maybe there is room for evolution to change the insertion site of the tendon or to bring another mechanism instead of the Achilles tendon in order to give efficient fast bipedal locomotion. Local tendons such as the plantaris, posterior tibial, peronis brevis and flexor digitorum longus can be used as transferred grafts in order to surgically mend Achilles tendon ruptures [30]. Maybe it is possible that one of these local tendons will eventually replace the Achilles tendon when it has reached its limit in an evolutionary sense. There are some signs of the Achilles tendon degenerating, as 7–20% of limbs are absent of the plantaris muscle, an important constituent muscle of the tendon [31]. So if the absent plantaris becomes more common among the human population, the Achilles tendon would lack its energysaving mechanism which would make walking and running more energy consuming. However other than for sports, the need for fast locomotion of humans is not as great as it used to be, which may mean that this energy saving mechanism in the Achilles tendon is no longer essential for human survival. So perhaps the Achilles tendon will degenerate further, until there is no longer a need for it. One example of a tendon that is disappearing from our anatomy is the palmaris longus. This tendon is absent in around 15% of people [32]. A study carried out on Asian subjects with and without palmaris longus’ found that there was no significant difference in their grip and pinch strengths [32]. Maybe this occurrence will be true for the Achilles tendon where its presence or absence will make no difference to bipedal locomotion in the due course of evolution. A single regulatory change in a gene that controls other genes can change how a gene network works, with dramatic consequences for the phenotype [33]. Homeobox genes encode proteins that bind and regulate the expression of DNA in multi-cellular organisms [33]. An example of homeobox gene is Ultrabithorax which regulates the development of the thorax segment in Drosophila by regulating pathways of at least thirty genes [34]. Mutations of the bithorax locus results in production of an extra set of wings [34]. This could occur in a human population if, for example environmental segregation occurs [34]. This would limit gene drift and would impose different selection pressures on the separated populations [34]. It would be possible that a homeobox gene that regulates the pathway of the gene controlling the embryological development of the Achilles tendon could be affected. This could then lead to a different phenotype (a double Achilles tendon, shorter/longer Achilles tendon, different insertion). If this new phenotype was less vulnerable to damage, then maybe these genes would be passed onto future generations and evolution of the Achilles tendon would continue on. Mokone et al. investigated whether there was a genetic predisposition to Achilles tendon pathology. They investigated 111 Caucasian subjects with Achilles tendon pathology and compared to 129 controls and were genotyped for variations in the COL5A1
gene [35]. The study concluded that COL5A1 BstUI restriction fragment length polymorphisms is associated with Achilles tendon pathology [35]. So it seems that genes do affect predisposition to Achilles tendinopathy. If the homeobox gene that regulates the COL5A1 BstUI was mutated, then may be this would lead to an Achilles tendon which is less prone to pathology. The TT genotype appears to be a protective against acute soft tissue ruptures. Three studies have suggested that rare TT genotypes of the functional sp1 binding site polymorphism with intron 1 of COL1A1 are associated with Achilles tendon rupture [36]. By understanding that there is a genetic influence on the predisposition for Achilles tendinopathy, maybe it is possible for genetic research to help athletes to be more resistant to Achilles tendon injuries [36]. 6. Conclusion In summary the Achilles tendon is here to stay in our anatomy. This is not only because of the evolutionary advantages its possesses such as facilitating fast bipedal locomotion, acting as a spring and shock absorber during gait, supplying an energy saving mechanism during movement and being the strongest tendon in the body. Another valid reason why this tendon will stay in our anatomy for many generations to come is because the rate of evolution in the human species is very slow [37]. Evolution is much slower in humans because they have out-competed other rivalry species like the Neanderthals and that humans themselves have altered the environment around them to their benefit [37]. Humans have exterminated big predators and natural selection is much slower in industrial populations that developing countries [37]. Factors that would affect human evolution would be viruses, artificial genetic modification or if humans altered the environment too much to their detriment [37]. So it seems that the Achilles tendon will be present in the human race for many generations to come. Therefore we should focus our efforts in carrying out research to help cope with its complicated pathology and improve the efficiency of its treatments. Future treatments could use genetic modification to prevent the predisposition to Achilles tendon pathology, and this could be special interest for the sporting fields. Aspenberg found that tendon repair can be stimulated by a single application of one of the several growth factors including PDGF, TGF-␣, IGF-1, VEGF and GDF-5,6,7, or by a thrombocite concentrate [38]. The response is dependent on the mechanical microenvironment, which is crucial for the repair process [38]. Hopefully in the future, medical knowledge will have advanced enough for us to overcome the evolutionary flaws of the Achilles tendon. Conflict of interest None. References [1] Montgomery S. Charles Darwin. http://www.christs.cam.ac.uk/darwin200/ pages/index.php?page id=c8; 2009. Christ’s College, Cambridge. 4-5-2011. [2] Hall BM. Science and evolution as science. In: Evolution principles and processes; 2010. [3] Hall BM. Human origins and evolution. In: Evolution principles and processes; 2010. [4] Kamrani K. The role of the Achilles tendon on the origins of bipedalism & human evolution. http://anthropology.net/2007/09/11/the-role-of-the2007. achilles-tendon-on-the-origins-of-bipedalism-human-evolution/; Anthropology.net. 4-5-2011. [5] Lesic A, Bumbasirevic M. Disorders of the Achilles tendon. Curr Orthop 2004;18(1):63–75. [6] Shirzad K, Hewitt JD, Kiesa C. Return to football after Achilles tendon rupture. http://www.lowerextremityreview.com/article/return-to-football-afterachilles-tendon-rupture; 2010. 4-5-2011.
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