This dissertation has been submitted by a student. This is not an example of the work written by our professional dissertation writers.
A Systematic Review of the physiotherapy management of lower limb tendonopathies
Tendonitis is a condition which is comparatively commonly seen in various clinics. The largest cohort of patients tend to have developed their condition as a result of various sports-related activities but it is acknowledged that there is a substantial cohort of RSI sufferers and occupation-related forms of tendonitis. (Kader et al 2002) In this piece we aim to review the various treatment modalities and to concentrate primarily on the eccentric muscle strengthening modalities of treatment, the rationale behind them and any evidence that they actually work.
Before we can consider the direct question of eccentric loading as treatment for tendonopathies we must examine the rationale for its uses well as the basic science and theory behind the actual practice. We will do this largely by the mechanism of a literature review.
In this review we shall be examining the literature for not only the methods that are currently employed in treating the various lower limb tendonopathies but also for justification for these methods and the quality of the science behind them. We shall therefore critically review the literature available and present it in a rational form.
In addition to this we intend to present an overview of various factors in a wider picture that are relevant to our considerations. We shall consider the current views on the pathophysiology of tendonitis and the experimental evidence on the response of the tendon to exercise in general terms.
Although it is accepted that the majority of patients currently seen in clinical practice with various forms of lower limb tendonitis are suffering from a sports related injury, we shall also look at the effects of ageing on tendon physiology as it is acknowledged that the elderly are another highly represented group with tendonitis.
We conclude the preamble with a number of clinical considerations, most prominently the difficulties posed by the differences in nomenclature and terminology which renders both assessments and comparisons between clinical trials difficult.
We conclude the dissertation with a review of various currently employed treatment modalities and the rationale behind them. We focus specifically on the use and place of eccentric muscle strengthening exercises in the spectrum of rational treatments..
Pathophysiology of tendonitis
At the macro-anatomical level, the tendon is usually easily defined as a semi-rigid white or grey structure, generally found in close proximity to synovial joints. One of its prime functions is to transmit forces generated by muscles to the skeletal system, often inducing movement. (Huxley HE 1979).
At the micro-anatomical level, it’s structure is very much more complex and requires a detailed examination before we can realistically and meaningfully consider the issues relating to the therapy of tendonitis.
Tendons form part of the anatomical structures that are functionally grouped together as the extracellular matrix (ECM). The rate of turnover – both synthesis and degradation – is influenced by a number of different factors including metabolic and disease related factors, but the strongest influence on the turnover rate is mechanical stress, usually as a result of various degrees of physical activity. (Agar Pet al 2000)
Tendon (and intramuscular) collagen, turns over at a rate which is about half as fast as myofibrillar protein turnover. The main physiological stimulus to turnover appears to be the multiple stimuli arising from mechanical or contractile activity.(Cuthbertson D et al2005)
At the cellular level, degradation of collagen is mediated largely byte metalloprotease group of enzymes and synthesis is most strongly influenced by a number of different trophic factors which are released at the cellular level. (Algren MS. 1999)
These growth factors are mainly responsible for both the transcriptional changes as well as the post-translational modifications that take place as a result of either physiological changes or disease processes. (Sand Meier et al 1997)
Until comparatively recently, tendon tissue was thought to be fairly inert. Recent research work has given good supportive evidence that the internal metabolic processes, the internal vascular responses (Alstom et al 1994) and the actual catabolic turnover of the collagen protein in response to physical activity, is considerably greater than originally thought. The converse is also true, as inactivity appears to have the same inhibitory effect on tendon tissue as the better known effect of wasting in muscle tissue. (Abrahamson SO et al 1996). This effect is of particular importance in our considerations (later) when we consider that some authorities suggest that outright rest is inappropriate initial treatment for tendonitis.
Collagen is a large polymer-type protein made up of many repeating subunits, (triple helices of polypeptides with a high proportion of proline and hydroxyproline). It is made by fibroblasts. In the muscle, it forms a basket-like network around the muscle fibres but then forms progressively more coherent and solid structure as it forms discrete tendon. In this way it allows the efficient transmission of forces generated by the myofibrils to the tendon – and hence to the bone. (Kjaer M 2004).
Training, in the form of physical work, exercise or repetitive movements, will have a trophic effect on the tendon as a whole. Collagen turnover can be increased and there can be an overall increase in the amount of collagen protein in the tendon. (Herzog W et al 2002)
Collagen, in the form in which it is found in a tendon, has enormous on-elastic tensile strength and a modest degree of ability to bend under lateral stress. As the amount of collagen in a tendon increases, the tendon’s mechanical (or more accurately, viscoelastic,) properties change. It decreases it’s stress levels for a given load, and thereby renders it more load resistant.(Fowls JL et al. 2000). Again this facts of great relevance to our clinical considerations later in this piece.
The stiffness, or resistance to lateral stress, is a function of the cross-linking of sulphur bonds across the parallel bands of protein. In general terms, the more cross-links, the stiffer the tendon. The degree of cross-linking is a result of a complex interaction between a number of enzyme systems in the matrix of the tendon. (Hamill OP et al.2001)
Polyglycans are an important feature of this enzyme cascade and become an increasingly important functional component as age increases. Older or ageing collagen will tend to exhibit glycolated cross links in addition to the sulphur links of youth. This is part of the reason why older tendons are less flexible (and possibly more prone to injury). (Inglemark BE 1948).
The functional significance of these links is that they render the tendon even stiffer and less able to bend.(Davidson PF 1989).Understanding these processes is fundamental to the prescribing of a rational treatment regime for tendon injuries and other pathologies.
It is also important to have a complete understanding of both the vascular and neurologically mediated adaptation processes that are present in the my-tendon complex. These work on a far more rapid and immediate time frame than the processes that we have just described, and are primarily responses to rapid changes in the mechanical loading stresses.
As muscle tissue develops physiologically, there is a symbiotic relationship between the muscle and the extracellular matrix. The various physiological mechanisms that stimulate muscle growth and hypertrophy appear to have a similar effect on the extracellular matrix. (MacLean et al 1991) But in the latter case, they are less well understood.
We know that that significant and repeated mechanical loading will trigger off, or initiate a process, which starts with the activation of trophic gene in a cellular nucleus, (Banes AJ et al.1999), it progresses through the complex processes of protein synthesis and functionally ends with the deposition of collagen in the tendon tissue.(Yasuda et al 2000)
Responses of the tendon to exercise
There would appear to be some form of integration between the muscular and the extracellular matrix signalling pathways, which optimises the co-ordinated activity of the trophic processes in response to the stimuli (which can be both loading and tensile in nature), which produce the response in the first place. (Viidik A.1993). This co-ordination mechanism must exist, as it is a well-recognised phenomenon that a tendon hypertrophies to accommodate the increased mechanical stress that its associated hypertrophied muscle produces. (Derwin et al 1999)
Considerable research effort has been expended in trying to delineate the mechanism, but to date, the results have not increased our understanding of the situation significantly. (Vierck J et al 2000)
Specific studies in this area have been able to show a clear correlation between collagen response and an increase in physical training. (Langberg et al 2001). The response was detectable after a 4week training programme and was maximal at 11 weeks.
When we consider the pathophysiology of RSI (repetitive strain injury) or even chronic overload syndrome, the stimuli that can produce muscle hypertrophy or increase muscle fibrosis can also produce fundamental changes in the tendon structure. (Birk DE et al 1990)
These changes can include changes in both the chemistry and the functionality of cross bonding of the collagen fibres, (Barnard K et al1987), changes in the size of the collagen fibrils, areas of locally increased blood flow (known as hyper vascularisation zones), and an increase in the catabolic processes which can result in either (or both) collagen being synthesised and laid down, or increase in fibroblastic activity which increases the fibrous component of the tendon.
(Greenfield EM et al 1999)
It is a fundamental recognition of the fact that these processes require “adjusted loading” rather than an enforced absence of loading(immobilisation) to reverse the physiological processes, that underpins most of the thrust of this review.( Howell JN et al 1993), (JärvinenTAH et al 2002)
The experimental evidence to support this view comes from the classic set of investigations by Gibson (et al 1987) who compared the rate of collagen synthesis and turnover in an immobilising long-cast leg with the rate of turnover in the unaffected leg. The rate of collagen synthesis dropped by half over a seven week period in the immobilised leg. The investigators also found an adaptive (and compensatory)reduction in the rate of collagen degradation which had the overall effect of reducing the protein loss in the tendons.
In the overall context of our investigation it is also important to note that the authors also found that minimal electrical stimulation of the muscle (5% of maximum voluntary contraction for 1 hr. per day),increased protein synthesis to such an extent that there was no net protein loss over the same seven week period of the trial. (Gibson etal 1989)
In a study that was remarkable for its invasiveness (the authors took repeated biopsies of human patella tendon after periods of exercise), Miller (et al 2004) demonstrated that tendon collagen synthesis showed a 30% rise within 6hrs of exercise and up to a 50%rise within a 24 hr. period. This was found to exactly follow the pattern of protein synthesis in skeletal muscle. This finding is strongly supportive of the assertions made earlier in this essay, that there would appear to be a mechanical or humeral mechanism that links the trophic effects that are apparent in both tendon and skeletal muscle.
Various authors have postulated different mechanisms (it has to be said - with scant evidence), including integrin’s, (Levenhagen et al2002), growth factors including transforming growth factor beta (TGFB) (Moore et al.2005), or mechano growth factor (MGF) (Rennie et al 2004),which they suggest may be responsible for the co-ordination of the trophic effects of perimysium collagen, tendon collagen and the myofibrils.
More concrete evidence exists (and is arguably of greater relevance to our investigation here), for the fact that dietary protein alone can produce a trophic stimulus for tendon collagen. (Jefferson &Kimball 2001). It is postulated that there is some form of amino acid sensor that is responsive to the availability of amino acids. This haste effect of changing the availability of various protein kinases in the extracellular matrix generally and a subsequent enzymatic cascade which results in an increase in various anabolic signalling molecules which are, in turn, responsible for the activation of mRNA. This is then responsible for the increased synthesis of collagen (and other related proteins), in tendon and other extracellular matrix tissues. This series of very elegant experiments was done in carefully controlled conditions which removed the possibility of other anabolic factors being relevant as the only variable was the availability of amino acids. (Cuthbertson et al 2005)
There is further evidence of the effect of exercise on tendon structure in the form of the set of experiments by Rennie and disco-workers. Looking specifically at the metabolism of collagen Rennie found that after strenuous exercise, the rate of incorporation of a marker into tendon collagen followed a specific pattern (Rennie &Tipton 2000). There was a latent period of about 90 mines after exercise where there was no change in metabolic rate. It was then noticed that there was a dramatic increase to about 5 times normal rates of synthesis, which peaked at about 12 hrs., was maintained for about 12hrs, and then declined over the next 48 hrs.
In line with the findings of Cuthbertson (above) the investigators noted that the rise in levels of synthesis is greatest if associated with an amino acid load just pre- or post-exercise, and this effect can be further enhanced by the administration of insulin secretagogues(such as glucose). There is therefore little doubt that feeding helps the post exercise response. (Atherton P et al 2005)
The effects of ageing on tendon pathophysiology
We have already commented, in passing, on the physiological effects of ageing in relation to the polyglycan cross bonding in tendons. There are a number of other changes which will naturally occur in relation to advancing years, which are of direct relevance to our considerations here. It is clearly a matter of observation that muscles, bones and tendons deteriorate as age increases. This deterioration leads to physical symptoms such as loss of strength, mobility and suppleness together with an increase in fatigability and a general reduction in proprioception. This condition is sometimes called “sarcopenia”.(Forbes 1987)
Epidemiological studies (Dorrens et al 2003), provide good evidence to support the popularly held view that an active lifestyle into old age is more likely to support a higher level of bone density, muscle bulk and tendon flexibility, than a sedentary one. One can postulate that the trophic mechanisms referred to above, stay active for longer when constantly stimulated by mechanical activity. One effect of ageing that has been experimentally demonstrated, is that the trophic effects of available amino acids in the bloodstream are not as great in the elderly as in the young. The elderly appear to have an ability to develop resistance to the trophic effects of amino acids, which was not present when they were younger. (Cuthbertson et al 2005)
Another physiological change that can be demonstrated in the elderly, is a reduced RNA : DNA ratio in tendon tissue, which is a marker of a reduced ability to manufacture protein. This, together with reduction in the amount of detectable anabolic signalling proteins, seems to be central in the failure of the muscle and tendon synthesising mechanisms. (Smack et al.2001).
If we add these findings to other work of Smack (et al 2001) and Leverhagen (et al 2002) which shows that the elderly can show responsiveness in terms of trophic changes in the collagen content of tendons by manipulation of the diet. Both studies showed that maximising the protein : energy ratio of ingested food is a reasonable strategy. It should also be noted that they also demonstrated that one has to be careful to keep the energy content of the food low in order to minimise unwanted weight gain.
The elderly could reasonably be assisted to maximise the benefit they get from training (resistance training in these particular studies), by integrating it with feeding concentrated in the immediate pre- or post-exercise period. This appears to have the effect of increasing the positive synergistic relationship between exercise and amino acid delivery.( Williams et al. 2002)
The first and possibly most fundamental issue that we have to consider when looking at the issues of the treatment of tendonitis, is the issue of correct diagnosis. This, sadly, is compounded by the fact that there appear to be several different terminology vocabularies in common clinical use. It therefore can be difficult to directly compare treatment studies of “tendonitis “ unless one has direct and clear diagnostic criteria. (Saxena 1995)
Tendonitis may be taken in some medical circles to include all those conditions which come under the broad heading of “painful overuse tendon conditions” (Khan et al 1999). This is generally accepted by the uncritical, as meaning that this equates with a painful inflammatory reaction in the tendon tissue. Histological investigation of the typical chronically painful tendon, generally shows an absence of the polymorphonuclear and other associated inflammatory cells. In some literature we can see the emergence and replacement of the term tendonitis with tendinitis. This latter term tends to be defined as pertaining to areas of collagen degeneration, increased ground substance and neo-vascularisation. (Purdue et al 1996)
To both illustrate and clarify the point, let us consider thevarious clinical entities that may either present like, or may be diagnosed as, “tendonitis”.
For ease of classification and clarity, in this section we shall consider the term “tendonitis” in specific relation to the Achilles tendon.
Williams (1986) produced the (arguably) most commonly currently accepted definitions of Achilles tendon pathologies. He classified them into:-
Per tendonitis (peritendonosis),
Other cases such as metabolic/rheumatic causes.
In common clinical parlance, any of them can be referred to, with reasonable accuracy, as “tendonitis”. (Galloway et al 1999)
The aetiologies can vary (and this may well have a bearing on treatment), from trauma, reduced flexibility, abnormal or changed biomechanical considerations (such as excessive pronation, supination or limb length inequalities) to name but a few. (Saxena, A 1998)
It should be noted that the anatomy of the Achilles tendon is unusual and certainly different from any other in the lower limb. It does not have a true synovial sheath but a petition which extends from its origin in the muscle to its insertion in the calcaneus. Peritendonosisis therefore a commonly misdiagnosed as Achilles tendonitis. It is also clinically significant that there is a region of decreased vascularity in the tendon, which is typically about 6 comes above its insertion (Hume 1994).
The clinical difference between these two conditions is that true Achilles tendonitis may, if chronic, be characterised by fucoid, or fatty focal degenerative, changes in the tendon itself, where asperitendonitis will not involve the Achilles tendon at all. (Kvist1994).
These degenerative changes may be extremely resistant to non-surgical forms of treatment. In practice, the two conditions may well be presenting the same individual. (Killer et al 1998)
The differentiating signs are, however, fairly easy to detect and the two conditions can be separately distinguished in most cases. Per tendonitis is the inflammation of the petition and can usually be clinically distinguished by the presence of clinical crepitus as the Achilles tendon tries to glide back and forth along the inflamed petition. This sign together with pain, generally tends to increase with activity and the tenderness is normally felt along the whole length of the tendon. Achilles tendonitis on the other hand classically gets better with movement and is at its worst after a period of rest. The discomfort tends to be more localised into discrete areas and is more commonly found in cases where there has been either a partial or even a complete rupture in the past. (Clement et al 1994)
Other pathologies can arise associated with the Achilles tendon, and for the sake of completeness we should briefly consider them as they could be potentially confounding factors in any trial which aims to consider tendonitis.
Tendocalcinosis is an inflammatory process which involves the Achilles tendon but only at the point of insertion to the calcaneal bone. It typically will result in calcification and therefore should be considered a different entity to Achilles tendonitis as such. It is characterised by localised pain, and prominence of the calcaneal insertion of the tendon which may well be associated with a retro-tendon bursitis. (Williams 1986)
If we apply the same rationale to the patella tendon, we are again faced with a bewildering array of terminology and conditions which tend to get lumped together as “tendonitis” and may also therefore be confounding factors in any study. We shall therefore spend a few paragraphs delineating them.
Some authors point to the fact that conditions that had been previously referred to as tendonitis, when examined at a histological level, are found to be the result of collagen breakdown rather than inflammation (Khan et al 1996), and therefore suggest the title oftendinosis is more appropriate. (Cook et al 2000) (I)
The whole issue of the role of the inflammatory process in the tendonopathies appears to be far from clear. An examination of the literature can point to work (such as that by Khan – above), who demonstrated that the prime histological changes were non-inflammatory and were more typical of fucoid, hyaline or fibrous degeneration with occasional calcific processes being identified. Other investigators however, point to the clinical picture which commonly includes the classic inflammatory triad of dolour, rub our and tumour (pain, redness and swelling)(Almekinders et al 1998). This, associated with the evidence of the relieving effect of NSAIA’s or corticosteroids(Friedberg 1997) leads to an ambiguous picture.
The pathophysiology of this condition is most commonly thought tube related to jumping and landing activity which is the mechanism which appears to cause the rupture of the collagen filaments and hence the histological appearances. The characteristics of this type of condition are that it tends to be focal, and often in the region of the lower pole of the patella. Initially it tends to be self healing but as the chronicity increases, the pain levels can increase to the point where pain is experienced even at rest (Cook et al 2000) (II)
This type of condition must clearly be differentiated from there-patella bursitis (Housemaid’s knee) which is often mistakenly diagnosed as a patella tendonitis.
(Halaby et al 1999)
Factors which appear to predispose to tendonopathy
Many authors identify chronic overuse as being one of the major factors in tendonopathy generally. (Kist 1994) (King et al 2000). This applies equally to the occupational tendonopathy as much as the sports-related conditions. (Jon stone 2000) (Kraushaar et al 1999). We should acknowledge that the term overuse can refer equally to overuse in terms of repetitive action just as much as it can refer to overloading. The two factors being independent (but often related).
Some of the current literature points to the fact that there can be differentiation in the spectrum of overuse injuries between those conditions that arise from some form of biochemical change in the structure of the tendon itself (Joss et al 1997), those that are associated with biomechanical changes (such as change in function or previous injury) (Alstom 1998) and those that arise as a result of ageing or other degenerative changes (Alstom et al 1995).
These factors can arise as a result of, or independently from, other factors such as the fact that the anatomical path of a tendon can take it over (or in close proximity to) friction-inducing structures such as a bony prominence – as in the case of the tibias posterior tendon, (Benjamin et al 1998) or factors relating to the site of insertion of the tendon into the bone – as in the case of theAchilles-calcaneum interface.(Benjamin et al 1995)
We can point to evidence that extraneous factors can also predispose to tendonopathy. There are genetic factors (Singer et al 1986), and a relationship to blood type (Joss et al 1989). The presence of certain concomitant chronic or debilitating illnesses can certainly be associated with tendonopathies (Kannur et al 1991) as can the chronic use of certain medications – most notably the fluoroquinolone group.(Huston 1994)(Ribard et al 1992). The mechanism in the latter case appears to be associated with an increase in the amount of MMP and its associated activity which seems to be associated with an increase in the rate of degradation of protein (especially collagen) in certain tissues. (Williams et al 2000).
Other authors have identified biomechanical factors as being significant (rather than necessarily causal), in the development oftendonopathies, but we shall discuss this in specific relation to treatment, and so will not discuss it further here
The spectrum of currently available treatment
Before beginning any rational consideration of the various forms of treatment available, one must appreciate a common truth in medicine, and that is that different treatments and different patients will respond differently to a specific treatment modality, and one of the factors that will influence this phenomenon is the skill and experience of the practitioner concerned. For example, a surgeon may well find that he gets good results from tenotomise but poor results from eccentric exercises and therefore will recommend surgery. Physiotherapist may find the converse. It is therefore important to be critical of such factors in any appreciation and appraisal of different techniques for the treatment of the lower-limb tendonopathies.
In this section we shall examine the available literature to try to obtain an overview of the various treatment modalities that are currently being prescribed and examine the rationale behind their use and efficacy
Most authors seem to agree that, before considering the specific conditions, a general approach of conservative measures (such as load reduction, strengthening exercises, and massage) should be tried before other modalities such as medication and physical interventions(ultrasound etc.), and that surgery should only realistically be considered as a last resort. The only obvious exception to that approach would be when complete (or sometimes perhaps partial ) rupture of the tendon has occurred, and then surgery may well be considered the prime intervention. (Cook et al 2000) (I)
Let us consider the various options in turn.
In this section we will begin (again, for the sake of clarity), by specifically considering the options available for patella tendonitis. We accept that there will, of course, be overlap between the treatments for the various tendonopathies, but it makes for a rational approach to consider each in turn.
The first comment that we must make is that, after examination of the literature it is noticeable that there are only a comparatively few well constructed, placebo controlled randomised trials in this area.(Almekinders et al 1998). Those that we can examine appear to suggest that the traditional treatments aimed at minimising the inflammatory processes in the condition are largely ineffective. The authors (Cooked al 2000) (II) suggest that this may well be because of the findings we have quoted earlier (Khan et al 1996) that histologically, the prime pathology is not inflammatory.
Cook (et al 2000) (I) points to the fact that many strategies can rationally involve load reduction and the (now outmoded) instruction to “Stop everything and rest” is positively contraindicated. The rationale for this relates to the mechanisms that we have examined earlier in this piece. Immobilisation of a tendon is actually harmful as we can point to evidence (above) that shows that tensile stress and mechanical action not only stimulates collagen production, it also is vital in tendon to ensure it’s optimal fibre alignment. Rational treatment suggests that a programme of “Relative rest” may be beneficial. By that, the authors (Cook et al 2000)(I) suggest that activity should continue as long as the prime traumas of jumping, landing or sprinting can be avoided and reintroduced in a carefully graded fashion.
Because patella tendonitis is primarily related to jumping and sprinting sports ( in numbers that present clinically), we will consider treatment in relation to them. The forces that are generated in the patella tendon on landing after a jump are considerably greater than those that produced the jump in the first place. (Richards et al1996). It logically follows that if biomechanical methods can be employed to more efficiently minimise the forces, they would be best employed on landing strategies than jumping ones.
One should appreciate that the energy-absorbing capacity of the limbs dependant, not only on the patella tendon, but factors at the hip and ankle as well.
Studies show that the ankle and calf are the prime sites of absorbing the initial landing load (Richards et al 1996) and, if these structures are not biomechanically sound, then this will increase the forces transmitted to the knee.
Prilutskii and his co-workers (et al 1993) completed a series of studies which showed that up to 40% of the energy absorbed on landing is transmitted proximally from the ankle/calf mechanism. It follows that it must be biomechanically sound if it is to absorb the 60% bulk of the load which otherwise would be transmitted upwards to the knee mechanism.
Another set of studies (Prapavessis et al 1999) concluded that when flat-foot and fore-foot landings were compared, the latter generated less forces throughout the lower limb and that the forces could be reduced further (up to another 25%) by increasing the range of both hip and knee flexion on landing.
There are a number of other potential biomechanical deficiencies that can be amenable to correction and should therefore be sought outspans planes may be an obvious anatomical problem detectable at an initial examination (Kaufman et al 1999), but there are other types of functional abnormality (such as excessively rapid pronation on landing) (McCrery et al 1999), that may require far more sophisticated evaluation. Outhouses inside shoes may go a long way to help these problems
Some authors, (McCrery et al 1999), regard a reduced range of movement in the sub-taller joints as an aggravating factor which places and undue stress on the Achilles tendon and that manual mobilisation of the joint is indicated in these cases.
In the light of the histological findings mentioned earlier,cryotherapy has a rational place in treatment. It is thought that it may help to reduce the development of new capillary beds in the affected tissue and also have a direct effect on the extravasation of both blood and zero-protein which is seen to occur histologically in this condition
(Riven burgh 1992). The reduction in temperature will also decrease the metabolic rate of the tissues and may therefore act as another factoring healing
(Pelletier et al. 1994)
This has been used empirically from time immemorial (Pelletier et al.1994). There have only been a few proper studies to confirm its efficacy, as it is clearly difficult to standardise any entry cohort and also standardise any particular form of massage. Most experienced healthcare professionals would however, attest to its pain relieving properties.
Some recent studies, however, have helped to clarify the therapeutic situation for us.
Davidson(et al 1997) demonstrated that deep friction massage promoted healing in the long tendons in rats and also maintained tissue compliance during the recovery period, and Gilson (et al 1999), was able to show the massage stimulated fibroblast production in inflamed tissue.
Alfred son (2005) in his tour de force paper on the treatment of Achilles tendonopathies recommends soft tissue massage (below the pain threshold) on a purely empirical basis to “maximise transverse mobilisation” but he does not refer to any rationality or justification for this statement.
There is better and more convincing evidence that ultrasound is beneficial in the treatment of tendinopathies. Ramirez and his colleagues (et al 1997) were able to demonstrate not only an increased fibroblast response, but also an increase in collagen deposition in controlled study.
Other workers have been able to demonstrate contributory evidence that ultrasound is able to increase both the eventual (post-healing) tensile strength and speed of healing in a tendon that has been surgically severed (Enwemeka 1990). A similar study had an incidental finding that ultrasound had little effect on the inflammatory processes that were present. (Enwemeka 1989)
It should be noted that these studies however, were tissue and animal based and may therefore not be directly applicable to the human condition. There is an additional complication and that is that there does not appear to be any universally accepted “normal therapeutic range” of ultrasound treatment or evaluation of an optimal dose, and this again makes comparative studies very difficult.
(Almekinders et al 1999)
NSAIA’s – Anti-inflammatory agents.
NSAIA’s have been empirically prescribed for tendonitis for years, but there is little reputable evidence to support their use. It is sobering to reflect that Almekinders and his team (et al 1999) found that NSAIA’s had virtually no effect on the healing rate of an inflamed tendon. (The same study also found no benefit from ultrasound either).
A larger study (Åstrom et al 1992) specifically looked at the value of piroxicam in Achilles tendonopathy and found that there was no demonstrable benefit.
Steroid injections have been used, but their use is fraught with difficulty. It is known that corticosteroids can significantly damp down inflammation in the body (Shirer et al 1996) however, in tendons they are known to be able to cause focal tissue necrosis. (Kraushaar etal 1999).
Shirer (et al 1996) point to the fact that there are currently no published studies that evaluate the possible benefits of steroid injection in this condition. What evidence we can find, points to one study which shows a demonstrable reduction in size of an inflamed tendon after the injection of steroid. This was a small study and the tendon size was measured by ultrasound which is not a precise instrument at this level of resolution (Clemens et al 1998).
A related study by the same workers was able to correlate this size reduction with a reduction in pain levels. (Pfeiffer-Jensen et al1998). It should be noted that although this particular study was small, it was placebo controlled.
One of the commonly recognised problems with the injection of steroids is the fact that there is an increased incidence of tendon rupture in the weeks after the injection has been given, so a warning of avoidance of maximal stress for some time must accompany this particular treatment. (Friedberg 1997)
Proteolysis enzyme inhibitors
This group of medications have only recently been introduced into the marketplace and therefore it is perhaps premature to draw specific conclusions about their efficacy. Early studies (Camass et al 1997)show a promising degree of apparent response. We shall have to await further longer-term evaluation.
We have found one reference to an authority (Beenak 2003) who advocates water-based therapy for tendonitis problems. It has to be said that this particular paper, although the clinical case had a very successful outcome, was based on a very small sample, (one), and offered no scientific rationale for its recommendations. It’s major justification was that it allowed for the athlete to exercise over full range of movements in a non-weight-bearing situation. From the “first principles” approach that we have adopted in considering the physiological basis for therapy, it is difficult to see how this can be considered beneficial in the treatment of the underlying pathology. We cannot therefore regard it as a rationale for mainstream therapy.
At this stage it should be conceded that there are some advocates of particular surgical procedures. It has to be said that surgery is probably not the treatment of first choice in the majority of tendonitis cases. Some authors suggest that surgery is to be recommended for those cases where conservative treatment fails. In teak, about 25% of cases of tendonitis eventually have some sort of surgical procedure. (Saxena A 1995). As this piece is primarily concerned with the physiotherapy modalities of treatment we shall not explore this area further
These types of intervention have also been frequently used, and withstood the test of time. (Clement et al 1984). They appear to be effective for most types of lower limb tendonopathy, but particularly so in Achilles tendonitis (Alfred son et al 1998), conditions of the patella tendon, and adductor tendonitis (Holmic et al 1999).
Because this type of programme is firmly in the realms of the physiotherapist’s expertise, we shall consider it in rather more detail.
There is often unease about deciding the appropriate timing of the commissioning of a strengthening programme, as there is clearly a matter of professional judgement as to when the particular exercise is not going to aggravate the problem and actually benefit it. It is presumably primarily for this reason that there is an apparent dearth of comparative trials in this area. Most experienced healthcare professionals would agree that even athletes with quite severe degrees of tendonitis can tolerate a modest strengthening programme. (Visentiniet al 1998)
With specific regard to patellar tendonitis, standing calf raises and isometric quadriceps strengthening exercises should be tolerated without too much difficulty. (Niesen-Vertommen et al 1992). The authors suggest that pain should be a guide to the amount of work that patient is advised to do in any particular circumstance.
This is a view shared by other workers in the field. (Valentine et al 1998)
It is a common clinical finding that patients who have lower limbtendopathies, will tend to favour the affected limb and transfer disproportionate amount of effort onto the unaffected leg. The prime mechanism for this phenomenon is the avoidance of pain, but it has the unwanted side effect of allowing muscle weakness to occur in the affected leg. The therapist must not only be aware of this, but must ideally assess the abnormal motor patterns that may develop and become quite entrenched, and provide appropriate exercises and mechanisms to counteract this effect.
Khan ( et al 1998)
Some workers in the field advocate the use of quadriceps exercises(viz. leg extensions), in patellar problems, with the aim of avoiding the masking use of the calf and gluteal muscles (Channel 1992). Other authors advocate the use of a squatting exercise on a 30’ decline board, as this also has the desired effect of slowing the impact of the calf muscles on the overall movement of knee flexion (as compared to a more usual squatting exercise with the feet flat on the ground).(Vailas et al 1995).
As the clinical condition improves, the healthcare professional can both speed up and add increased loading to the exercise in order to maximise the benefit and finally the patient can then be encouraged to improve endurance. The same author makes comment on eccentric exercises. As we are to consider this modality in more detail shortly, we should note that they specifically recommend that such exercises are left to the end of the treatment regime as they have been known to produce tendon pain if introduced to the regime too early.
Cannel (1992) also observes that there are several mechanisms for failure in these types of regimes. Generally they fail because progress through the speed or loading scales can be too fast and the eccentric exercises may be introduced either too early or perhaps too aggressively. It is also good clinical practice to advise that the exercises are continued beyond the return to actual sport or activity. In short, it is a matter of considerable skill, judgement and experience to get the best result in a given clinical situation.
Eccentric muscle exercises are currently being recommended as another adjunct to a training regime in cases of tendonitis.
In most normal movement, an eccentric movement precedes a movement in the intended direction (concentric movement). This combined cycle of both eccentric and concentric movements is known as a stretch shortening cycle. (Grantham 2005).
Another definition of eccentric strength is the ability to resist muscle lengthening Walkman (2000)
The significance of the eccentric phase of the movement is that performance in the concentric movement is enhanced by extra loading of the preceding eccentric movement. To give a specific example it can be shown that additional loading added in the eccentric phase of a standard weight lift will actually increase the amount of weight that weight lifter can manage to raise in the concentric phase of the contraction. (Grantham 2005)
To put this in perspective it is instructive to consider particularly elegant and well-designed study by McCrery (et al 1999),which set out to carefully compare the biomechanics of one cohort or runners who had chronic Achilles tendonitis with another group that were otherwise matched but symptom-free.
There were two major differences that were found between the two groups and they were in the strength of the dorsa- and plantar-flexors of the foot (measured with an isokinetic dynamometer), and the degree of pronation. The symptomatic group had significantly weaker flexors and had a greater average in the amount of pronation. It has to be said that this team were extremely thorough in their biomechanical assessments, and they could detect no other statistically significant differences between the two groups.
The authors suggested that it was therefore rational to recommend strengthening exercises specifically targeted at the dorsa- and plantar-flexors and in-shoe orthotics to help to reduce the amount of rear foot pronation that occurred in the running cycle.
It is worth considering these recommendations in a little more detail as they appear to be based in good science. The authors postulate that it is a basic lack of strength in the gastrocnemius and soleus muscles (which give rise to the Achilles tendon ) that results in an insufficient degree of control of the ankle joint when the foot strikes, and subsequently settles on, the ground. Their study showed that it is the calf muscles that are the primary mechanism for absorbing the forces from the first part of the impact with the ground.
We stress this point here, because it is at this point that the calf muscles are actually working eccentrically in trying to control the forward movement element in the lower part of the leg. At the same time (during first impact), the tibias anterior muscle is also working in an eccentric fashion to try to limit the amount of pronation that is occurring as the foot adapts to the flat, mid-cycle phase. Awe have outlined earlier, it is during the eccentric phase of contraction that the musculo-tendonous unit is lengthening against resistance. (Testis et al 1993)
It is this understanding of the biomechanics of the lower leg that underpins much of the author’s rationale for treatment.
We should observe that this set of observations (however meticulously carried out) does not constitute a firm proof of a causal relationship between tendonitis and excessive pronation and weak musculature. It actually does no more than simply quantify the differences between those people who have problems and those who don’t, but the statistically significant differences between the two groups is more than sufficient evidence on which to base sound “evidence based” practice.
In order to understand the mechanism in a little more detail, we should consider the normal actions of the pronating foot during the running cycle. Pronation actively absorbs some of the impact forces as the foot contacts the ground. Pronation (to a degree) is therefore abnormal, physiological activity of the foot during the impact phase. It follows that over pronation has the biomechanical effect of over-rotation of the lower leg in an inward direction.
The corollary of this is that when the patient moves on to the take-off segment of the pace, with the ankle extending (the concentric phase of the calf muscle cycle), the muscles and tendons that act over the ankle joint are not then optimally placed to exert an efficient force transmission. The Achilles tendon takes the lion’s share of this force (by virtue of the fact that it is attached to the strongest muscles), and it therefore follows that greater stress is placed upon the Achilles tendon.
Brandenburg and his colleagues (et al.2002) take a slightly different emphasis. They regard the critical motion as the eccentric contraction which occurs in the calf muscle complex after the foot is flat on the ground. They state that it is the dorsiflexion that occurs ( at the ankle, as the lower leg comes over the foot) that is often the movement that is primarily responsible for the tendonitis and that the forces generated in the Achilles tendon are greater if there is an excessive degree of pronation at the level of the ankle.
They make the suggestion(quite logically) that it is this level of excessive dorsiflexion(and/or pronation) which results from an inadequately strong calf muscle complex that not only gives rise to the factors that cause Achilles tendonitis, but that it also ruins the running economy as extra energy must be utilised to compensate to correct the biomechanically inefficient movements. They suggest that it is this extra energy which causes the problems with the tendon.
It is therefore a logical extension of this argument that strengthening the calf muscles eccentrically actually makes them more efficient in bringing both the elements of excessive dorsiflexion and pronation under control. This therefore reduces the strain on the Achilles tendon and reduces the predisposition to tendonitis.
This argument is not new however. Standish (et al 1986) wrote an article which is regarded as a classic by many. His theory came from slightly different angle to those that we have just discussed. He believed that if excessive eccentric loading was the root cause of the micro- (or sometimes macro-) tearing that occurred in a tendon (not just the Achilles tendon) then it seemed logical that a treatment programme should include eccentric strengthening exercises. Not only does he advocate eccentric exercises for Achilles tendonopathies but also quadriceps eccentric exercises for patella tendonopathies (with the same rationale.)
Fyfe (et al 1992) expanded on the work of Standish, and made the comment
"The maximum stress placed upon the muscle-tendon unit is during eccentric exercises, and only if one can strengthen the muscle-tendon unit to withstand these stresses will it be able to cope and prevent injury. Isometrics and concentric exercises have their place, but only through eccentrics will the maximum achievement be attained."
Both authors pointed to a previous study by Kami (et al 1972) who contrasted three groups of subjects – all with Achilles tendonitis –with different modalities of treatment (concentric, eccentric and no exercises). His findings were (in essence):
The eccentric group on a percentage basis showed a greater increase in maximum tension than the concentric group in all concentric, eccentric, and isometric tensions, although it took the eccentric group longer time to reach the maximal isometric tension relative to the concentric group.”
The reason that we have examined this particular issue in greater depth is that it provides that rationale for the eccentric strengthening exercises. It follows that a calf mechanism that can be stronger under conditions of eccentric contraction, will allow less of an excessive pronation during foot-strike and follow through. For the reasons that have been set out above, this then equates with less of force being transmitted through the Achilles tendon during the take-off phase of the cycle.
Walkman (2000) (a respected authority in this field), has developed graduated system of eccentric exercises which have been widely adopted by the physical therapy community as being the “gold standard “of eccentric exercises in the area of leg tendonopathies (Alfredson2005)
The Walkman programme is widely available and so we shall not specifically detail it here. One of the characteristic features ofWallmann’s programme however, is the emphasis on “bent-knee” eccentric strengthening. The rationale behind this is to focus the bulk of the activity on the soleus muscle which (by virtue of its anatomy) tends to pull the Achilles tendon slightly more medially than the gastrocnemius, and thereby it helps to further combat the effects of over pronation. Alfred son however, advocates the use of both bent and straight knee eccentric exercises if over pronation is not a clinical problem
Alfred son (2005) has slightly modified the Walkman programme to make it rather more aggressive, and it places greater reliance on building up the loading stresses rather than speed at the expense offloading. Alfred son argues that this is more effective at producing the desired strength changes in the muscle. (Alfred son et al 1998). It should be noted that this method is only really suitable for patients who are able to tolerate single leg loading exercises at the beginning of the treatment programme.
The same author also makes the comment that eccentric exercises have the potential to actually cause damage if used overzealously or inappropriately. he advises that they should always be preceded by an appropriate warm-up routine and commenced gently before increasing either load or speed to maximal therapeutic levels. The therapeutic regime notes that a patient should normally experience degree of pain at the beginning of each programme and with the addition of a new loading pattern. The particular exercise rate should be maintained until pain-free before progressing to the next loading level.
To return to consider the science behind the theory. Alfred son tested his regime with cohorts of patients matched for symptom severity and randomly allocated them either to a 12 week eccentric exercise programme, or to surgery. The results were that both groups had almost equally matched results in terms of both speed of return to activity and also degree and speed of pain relief. This therefore shows that surgical results can be at least matched by non-invasive (and therefore less risky) procedures. For reasons that the authors do not amplify, they observe that their treatment regime appears to be maximally effective in the “early forties” age group.
Some other authors and investigators have suggested modifications of this basic model of programme. Some, (Mortensen et al. 1999) will advocate doing the eccentric phase of the exercise with the patient leaning up against a wall. They argue that this has the merit of allowing less than maximal body-weight forces to be generated in the early stages of the treatment plan. Obviously the greater the angle between the body and the wall, the less force is generated by the bodyweight, but equally the degree and range of stretch is greater. This mechanism is recommended to be inserted in the regime before the eccentric exercise on a step, which allows the full body-weight to be supported and the calf muscle to be maximally stretched by allowing the heel to descend below the level of the toes.
Some authors, (Waterson et al 1997) advise the additional measure of an Air cast pump to help to massage the avascular area of the Achilles tendon. They believe that it helps to increase vascularity in this region. It has to be said that we cannot find any good quality trials to support this clinical impression.
Other authors (Payola et al 2000) advocate the use of post-exercise ice to help to minimise the discomfort and/or swelling that the exercise may generate
As with all evidence-based practice, one has to reflect on one’s own practice
Gibbs (1998) and contrast it with a critical evaluation of the evidence in the literature. The purpose of this evaluation is to provide such critical overview. In undertaking this review, we have presented the pathophysiology that is related to the tendon pathologies and have assessed various opinions with regard to appropriate treatment.
There is clearly conflicting evidence as to the place that NSAIA’s haven treatment with some authorities advocating their use and others who cannot find any evidence for efficacy. This may be a reflection of the potential difficulties that we have identified in the trial entry criteria with different nomenclature and indeed, different possible interpretations of pathology.
It would seem that injectable steroids are fraught with difficulty and therefore are probably best avoided. We have not been able to find convincing evidence to support the use of ultrasound in the varioustendonopathies. Some authorities have advocated the use of ice, bothin the acute phase of injury and as an adjunct to treatment and there does seem to be a sound basis to recommend this.
Strengthening exercises do seem to be almost universally recommended and the specific use of eccentric muscle exercises is not only recommended but has a wealth of pathophysiological and experimental data to back it up. We would feel confident, on the basis of the evidence that we have presented, in saying that eccentric muscle exercises probably would form the backbone of any rational treatment or rehabilitation package that should be offered to a patient with lower limb tendonopathy.
We have explored the field of biomechanics. It impinges upon the rationale for recommending eccentric exercises and we have discussed this is great detail. Elsewhere in the field of biomechanics we have looked at the correction of possible jumping and landing techniques and the possible use of orthotics. All these factors may well have a place in specific cases.
We have considered the surgical option only in passing. Most of the authorities that we have reviewed, are of the opinion that surgery is best reserved for resistant cases where conservative treatment has failed. This seems to be on the basis that we have pointed to evidence which shows that eccentric strengthening exercises are at least as effective as surgery on a percentage basis for all cases. This comments clearly made in the light of the clear exceptions to this such as tendon rupture etc.
Reflection on the issue suggests that, as in most fields of medicine, it is not simply a matter of assembling sound evidence and prescribing appropriate treatment. One must also consider both the holistic approach to patient well-being (Kuhse et al 2001) and also the issues of empowerment and education of the patient (Marinker 1997).
It is clearly no value in clearing up an old lady’s painful Achillestendonitis in the clinic if she is discharged straight back to having to carry her shopping home up a steep hill. Equally it is of little value in pontificating about the value of eccentric exercises in anyone particular case. Much greater benefit will be obtained if one can explain to the patient the reasons and the rationale behind just why ascertain type of treatment is being selected for their particular case.
In broad terms, we have approached this issue from a rational and scientifically rigorous viewpoint. This should not blind us, as practitioners, to the fact that as well as being a science, most fields of medicine are also practised as an art. We may be able to base our practice on sound scientific principles but also we should accept that there is no substitute for experience and judgement in any one individual case.
Agar P, Simonise EB, Andersen JL, Magnusson SP, Halkjær-Kristensen J, and Dyhre-Poulsen P. 2000
Neural inhibition during maximal eccentric and concentric quadriceps contraction: effects of resistance training.
J Appl Physiol 89: 2249–2257, 2000.
Algren MS. 1999
Matrix metalloproteinases (MMPs) are required for re-epithelialization of cutaneous wounds.
Arch Dermatol Res 291: 583–590, 1999.
Åstrom M, Westlin N. 1992
No effect of piroxicam on achilles tendinopathy. A randomized study of 70 patients. Acta Orthop Scand 1992; 63: 631–4.
Aaström M and Westlin N. 1994
Blood flow in chronic Achilles tendinopathy.
Clin Orthop 308: 166–172, 1994.
Aaström M and Rausing A. 1995
Chronic Achilles tendinopathy: a survey of surgical and histopathological findings. Clin Orthop 316: 151–164, 1995
Aaström M. 1998
Partial rupture in chronic Achilles tendinopathy. A retrospective analysis of 342 cases.
Acta Orthop Scand 69: 404–407, 1998
Abrahamson SO and Lohmander S. 1996
Differential effects of insulin-like growth factor-1 on matrix and DNA synthesis in various regions at types of rabbit tendons.
J Orthop Res 14: 370–376, 1996.
Alfred son H, Pietila T, Jonsson P, et al: 1998
Heavy-load eccentric calf muscle training for the treatment of chronic Achilles tendinitis.
Am J Sports Med 1998;26(3):360-366
Alfred son H 2005
Pain in the Achilles Region
Clinical Sports Medicine. 2005, Chapter 28
Almekinders LC, Temple JD: 1998
Etiology, diagnosis, and treatment of tendonitis: an analysis of the literature.
Med Sci Sports Exerc 1998;30(8):1183-1190
Almekinders LC, Deol G: 1999
The effects of aging, anti-inflammatory drugs, and ultrasound on the in vitro response of tendon tissue.
Am J Sports Med 1999;27(4):417-421
Atherton P, Babraj J, Smith K, Rennie M & Wackerhage H (2005).
Selectiveactivation of AMP PGC-1 signalling can explain specific adaptiveresponses to endurance or resitance training-Iike electrical musclestimulation. FASEB J 19, 786–788 2005
Banes AJ, Horesovsky G, Larson C, Tsuzaki M, Judex S, Archambault J, Zernicke R, Herzog W, Kelley S, and Miller L. 1999
Mechanical load stimulates expression of novel genes in vivo and in vitro in avian flexor tendon cells.
Osteoarthritis Cartilage 7: 141–143, 1999.
Barnard K, Light ND, Sims TJ, and Bailey AJ. 1987
Chemistry of the collagen cross-links: origin and partial characterization of a putative mature cross-link of collagen.
Biochem J 244: 303–309, 1987.
Benjamin M, Qin S, and Ralphs JR. 1995
Fibrocartilage associated with human tendons and their pulleys .
J Anat 187: 625–633, 1995
Beenak, P C Malliou and G Benekas 2003
Water and land based rehabilitation for Achilles tendinopathy in an elite female runner
Br J Sports Med 2003;37:535-537
Benjamin M and Ralphs JR. 1998
Fibrocartilage in tendons and ligaments: an adaptation to compressive load.
J Anat 193: 481–494, 1998
Birk DE, Fitch JM, Babiarz JP, Doane KJ, and Linsenmayer TF. 1990
Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter.
J Cell Sci 95: 649–657, 1990.
Brandenburg, J.P. and Docherty, D. (2002)
The effects of accentuated eccentric loading on strength, muscle hypertrophy, and neural adaptations in trained individuals.
Journal of Strength and Conditioning Research 16, 25-32.
Cannel LJ: 1982
The effects of an eccentric-type exerciseversus a concentric-type exercise in the management of chronic patellartendonitis, thesis.
Vancouver, British Columbia, University of British Columbia, 1982
Camass G, Testa V, Maffulli N, et al:1997
Aprotinin, corticosteroids, and normosaline in the management ofpatellar tendinopathy in athletes: a prospective randomized study.
Sports Exerc Inj 1997;3(2):111-115
Clement DB, Taunton JE, Smart GW: 1984
Achilles tendinitis and peritendinitis: etiology and treatment.
Am J Sports Med 1984;12(3):179-184
Clement, D. B., Taunton, J. E., Smart, G. W. 1994
Achilles Tendinitis and Peritendinitis: Etiology and treatment.
Am. J. Sport Med. 12:179-184, 1994.
Clemens D, Pfeiffer-Jensen M, Friedberg U, et al: 1998
Ultrasonographic visualisation of inflamed tendons before and after local glucocorticosteroid
Scand J Rheumatol 1998;41(suppl):27
Cook, Khan, Maffulli & Purdam 2000 (I)
Overuse Tendinosis, Not Tendinitis
The Physician and Sports Medicine Vol.28 No6. June 2000
Cook JL, Kiss ZS, Khan KM, et al: 2000 (II)
Reproducibility and clinical utility of tendon palpation to detect patellar tendinopathy in young basketball players.
Br J Sports Med 2000,
Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage et al. (2005).
Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 19, 422–424 2005
Davidson PF. 1989
The contribution of labile cross-links to the tensile behaviour of tendons.
Connect Tissue Res 18: 293–305, 1989
Davidson CJ, Ganion LR, Gilson G, et al: 1997
Rat tendon morphological and functional changes resulting from soft tissue mobilization.
Med Sci Sports Exerc 1997;29(3):313-319
Derwin KA and Soslowsky LJ. 1999
A quantitative investigation of structure-function relationship in a tendon fascicle.
J Biomech Eng 121: 598–604, 1999.
Dorrens J & Rennie MJ (2003).
Effects of ageing and human whole body and muscle protein turnover.
Scand J Med Sci Sports 13, 26–33. 2003
Enwemeka CS. 1989
The effects of therapeutic ultrasound.
Am J Phys Rehabil 1989; 68: 283–7.
he effects of therapeutic ultrasound on tendon healing: a biomechanical study.
Am J Phys Med Rehabil 1990;69(5):258]
Smack B, Andersen JL, Olsen S, Richter EA, Mizuno M & Kjaer M (2001).
iming of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans.
J Physiol 535, 301–311. 2001
Forbes GB (1987).
Human Body Composition: Growth, Aging, Nutrition and Activity, 1st edn, 171 pp. New York: Springer-Verlag, New York.1987
Fowls JL, MacDougall JD, Tarnapolsky MA, Sale DG, Roy BD, and Yarasheski KE. 2000
The effects of acute passive stretch on muscle protein synthesis in humans.
Can J Appl Physiol 25: 165–180, 2000.
Friedberg U: 1997
Local corticosteroid injection in sport: a review of literature and guidelines for treatment.
Scand J Med Sci Sport 1997;7(3):131-139
Fyfe I, Standish WD: 1992
The use of eccentric training and stretching in prevention of tendon injuries.
Clin in Sports Med., 11(3):601-624,1992.
Galloway, M. T., Jokl, P., Dayton, D. W. 1999
Achilles tendon overuse injuries. In Clinics in Sports Medicine,pp.771-782, edited by P. Renstrom and Wayne Leadbetter, W. B. SaundersCo.,
Philadelphia: Philadelphia publishing Ltd, 1999.
Gilson G, Ganion LR, Helfest R: 1999
Fibroblast response to variation in soft tissue mobilization pressure.
Med Sci Sports Exerc 1999;31(4):531-535
Gibbs, G (1998)
Learning by doing: A guide to Teaching and Learning methods
EMU Oxford Brookes University, Oxford. 1998
Gibson JNA, Halliday D, Watt PW, Stoward PJ, Morrison WL & RennieMJ (1987). Decrease in human quadriceps muscle protein turnoverconsequent upon leg immobilisation.
Clin Sci 72, 503–509. 1987
Gibson JN, Morrison WL, Scrimgeour CM, Smith K, Stoward PJ & RennieMJ (1989). Effects of therapeutic percutaneous electrical stimulationof atrophic human quadriceps on muscle composition, protein synthesisand contractile properties.
Eur J Clin Invest 19, 206–212. 1989
Grantham N 2005
Eccentric muscle exercises
Journal of Strength and Conditioning Research, vol 16 (1), pp 9-13 2005
Greenfield EM, Bi Y, and Miyauchi A. 1999
Regulation of osteoclast activity.
Life Sci 65: 1087–1102, 1999.
Hamill OP and Martinac B. 2001
Molecular basis of mechanotransduction in living cells.
Physiol Rev 81: 685–740, 2001
Herzog W and Leonard TR. 2002
Force enhancement following stretching of skeletal muscle: a new mechanism.
J Exp Biol 205: 1275–1283, 2002.
Holmic P, Uhrskou P, Ulnits L, et al: 1999
Effectiveness of active physical training as treatment forlong-standing adductor-related groin pain in athletes: randomisedtrial.
Howell JN, Chelboun G, and Conaster R. 1993
Muscle stiffness, strength loss, swelling and soreness following exercise-induced injury in humans.
J Physiol 464: 183–186, 1993.
Hume, E. L. 1994
Traumatic disorders of the ankle or overuse syndromes. In Traumatic Disorders of the Ankle, pp 56-58, edited by W. C. Hamilton,
New York: Springer Verlag, New York, 1994
Achilles tendinitis and tendon rupture due to fluoroquinolone antibiotics.
N Engl J Med 331: 748–749, 1994
Huxley HE. 1979
The mechanism of muscular contraction.
Science 164: 1356–1366, 1979
Inglemark BE. 1948
The structure of tendons at various ages and under different functionalconditions. II. An electronmicroscopic investigation from white rats.
Acta Anat 6: 193–225, 1948.
Järvinen TAH, Joss L, Kannur P, Järvinen TLN, and Järvinen M. 2002
Organization and distribution of intramuscular connective tissue in normal and immobilized skeletal muscle.
J Muscle Res Cell Motil 23: 245–254, 2002.
Jefferson LS & Kimball SR (2001).
Translational control of protein synthesis: implications for understanding changes in skeletal muscle mass.
Int J Sport Nutr Exerc Metab 11 (suppl.), S143–S149. 2001
Jon stone AJ. 2000
Tennis elbow and upper limb tendinopathies.
Sports Med Arthroscop Rev 8: 69–79, 2000.
Joss L, Balint BJ, Kannur P, Reffy A, and Barzo M. 1989
Distribution of blood groups in patients with tendon rupture. An analysis of 832 cases.
J Bone Joint Surg 71: 272–274, 1989.
Joss L and Kannur P. 1997
Human Kinetics, 1997, p. 1–576.
Kader D, Saxena A, Movin T, et al. 2002
Achilles tendinopathy: some aspects of basic science and clinical management.
Br J Sports Med 2002;36:239–49
Kannur P and Joss L. 1991
Histopathological changes preceding spontanous rupture of a tendon. A controlled study of 891 patients.
J Bone Joint Surg 73: 1507–1525, 1991.
Kaufman KR, Brodine SK, Shaffer RA, et al: 1999
The effect of foot structure and range of motion on musculoskeletal overuse injuries. Am J Sports Med 1999;27(5):585-593
Khan KM, Bonar F, Desmond PM, et al: 1996
Patellar tendinitis (jumper's knee): findings at histopathologicexamination, US and MR imaging: Victorian Institute of Sport TendonStudy Group.
Khan KM, Maffulli N, Coleman BD, et al: 1998
Patellar tendinopathy: some aspects of basic science and clinical management.
Br J Sports Med 1998;32(4):346-355
Killer WB, Herring SA, Press JM, et al. 1998
Functional rehabilitation of sports and musculoskeletal injuries. Gaithersburg, MD: Aspen Publishers Inc, 1998:273–83.
King JB, Cook JL, Khan KM, and Maffulli N. 2000
Sports Med Arthroscop Rev 8: 86–95, 2000
Kjaer M (2004).
Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading.
Physiol Rev 84, 649–698
Kraushaar BS, Nirschl RP: 1999
Tendinosis of the elbow (tennis elbow): clinical features and findingsof histological, immunohistochemical, and electron microscopy studies.
J Bone Joint Surg (Am) 1999;81(2):259-278
Kuhse & Singer 2001
A companion to bioethics
ISBN: 063123019X Pub Date 05 July 2001
Kist, M., Jarvinen, M. 1994
Clinical histochemical and biomechanical features in repair of muscle and tendon injuries.
Int. J. Sport Med. 3 (Suppl) 1:12-14, 1994.
Kist M. 1994
Achilles tendon injuries in athletes.
Sports Med 18: 173–201, 1994
Langberg H, Rosendal L, and KjærM. 2001
Training induced changes in peritendinous type I collagen turnover determined by microdialysis in humans.
J Physiol 534: 397–402, 2001.
Levenhagen DK, Carr C, Carlson MG, Maron DJ, Borel MJ & Flakoll PJ(2002). Postexercise protein intake enhances whole-body and leg proteinaccretion in humans.
Med Sci Sports Exerc 34, 828–837
MacLean DA, Spriet IL, Hultman E, and Graham TE. 1991
Plasma and muscle amino acid and ammonia responses during prolonged exercise in humans.
J Appl Physiol 70: 2095–2103, 1991
From compliance to concordance: achieving shared goals in medicine taking.
McCrery JL, Martin DF, Lowery RP, et al: 1999
Etiologic factors associated with Achilles tendinitis in runners.
Med Sci Sports Exerc 1999;31(10):1374-1381
Miller BF, Olesen JL, Langberg H, Barbraj JA, Smith K, Rennie MJ, and Kjær M. 2004
Protein synthesis of muscle and tendon increases simultaneously following strenous exercise.
FASEB J. 2004
Moore DR, Phillips SM, Babraj JA, Smith K & Rennie MJ (2005).
Myofibrillar and collagen protein synthesis in human skeletal muscle inyoung men after maximal shortening and lengthening contractions.
Am J Physiol Endocrinol Metab 288, E1153–1159 2005
Mortensen NHM, Skov O, Jensen PE. 1999
Early motion of the ankle after operative treatment of a rupture of the Achilles tendon.
J Bone Joint Surg 1999: 81A: 983–90.
Niesen-Vertommen SL, Taunton JE, Clement DB, et al: 1992
The effect of eccentric versus concentric exercise in the management of Achilles tendonitis.
J Sport Med 1992;2(2):109-113
Payola M, Orava S, Leppilahti J, et al. 2000
Chronic Achilles tendon overuse injury: complications after surgical treatment. An analysis of 432 consecutive patients.
Am J Sports Med 2000; 28: 77–82.
Pelletier G, Hamel H, Behnke P: 1994
Treatment of infrapatellar tendinitis: a combination of modalities and transverse friction massage versus iontophoresis.
J Sport Rehabil 1994;3:1315-1345
Pfeiffer-Jensen M, Friedberg U, Clemens D, et al: 1998
Pain assessment in inflamed tendons before and after placebo and local glucocorticosteroid, abstracted.
Scand J Rheumatol 1998;41(suppl):146
Prapavessis H, McNair PJ: 1999
Effect of instruction in jumping technique and experience jumping on ground reaction forces.
J Orthop Sports Phys Ther 1999;29(6):352-356
Prilutskii BI, Zatsiorskii VM, Petrova LN: 1993
"Tendon" action of two-joint muscles during human locomotion: transferof mechanical energy between links in shock-absorbing and push-offphases [in Russian].
Purdue G, Ippoliro E, Postacchini F: 1996
A classification of Achilles tendon disease.
Am J Sports Med 1996;4(2):145-150
Ramirez A, Schwane JA, McFarland C, et al: 1997
The effect of ultrasound on collagen synthesis and fibroblast proliferation in vitro. Med Sci Sports Exerc 1997;29(3):326-332
Rennie MJ & Tipton KD (2000).
Protein and amino acid metabolism during and after exercise and the effects of nutrition.
Annu Rev Nutr 20, 457–483 2000
Rennie MJ, Wackerhage H, Spangenburg EE & Booth FW (2004).
Control of the size of the human muscle mass.
Annu Rev Physiol 66, 799–828. 2004
Ribard P, Audisio F, Kahn MF, De-Bandt M, Jorgensen C, Hayem G, Meyer O, and Palazzo E. 1992
Seven achilles tendinitis including 3 complicated with rupture during fluoroquinilone therapy.
J Rheumatol 19: 1479–1481, 1992
Richards DP, Ajeman SV, Wiley JP, et al: 1996
Knee joint dynamics predict patellar tendinitis in elite volleyball players.
Am J Sports Med 1996;24(5):676-683
Riven burgh DW: 1992
hysical modalities in the treatment of tendon injuries.
Clin Sports Med 1992;11(3):645-659
Sand Meier R, Renstrom RA F H. 1997
Diagnosis and treatment of chronic tendon disorders for the treatment of chronic Achilles tendinitis.
Scand J Med Sci Sports 1997;7:96–106
Saxena A 1995
Achilles tendon pathologies
Foot And Ankle Surgery Vol 3 1995.
Saxena, A. 1998
Achilles Peritendonosis: An unusual case due to frostbite in an elite athlete.
J. Foot & Ankle Surg. 1(33):87-90, 1998.
Halaby M, Almekinders LC: 1999
Patellar tendinitis: the significance of magnetic resonance imaging findings.
Am J Sports Med 1999;27(3):345-349
Shirer I, Matheson GO, Kohl HW III: 1996
Achilles tendonitis: are corticosteroid injections useful or harmful?
Clin J Sport Med 1996;6(4):245-250
Singer KM and Jones DC. 1986
Soft tissue conditions of the ankle and foot. In: The Lower Extremityand Spine in Sports Medicine, edited by Nicholas JA and Hershmann EB.
St Louis, MO: Mosby, 1986, p. 148–164.
Standish WD, Rubinovich M, Curwin S: 1986
Eccentric exercise in chronic tendinitis.
Clin Orth & Rel. Res., 208:65-68, 1986.
Testis CL and Lieber RL. 1993
Relationship between Achilles tendon mechanical properties and gastrocnemius muscle function.
J Biomech Eng 115: 225–230, 1993.
Vailas AC, Pedrini VA, Pedrini-Mille A, and Holloszy JO. 1995
Patellar tendon matrix changes associated with aging and voluntary exercise.
J Appl Physiol 58: 1572–1576, 1995
Vierck J, O'Reilley B, Hossner K, Antonio J, Byrne K, Bucci L, and Dodson M. 2000
Satellite cell regulation following myotrauma caused by resistance exercise.
Cell Biol Int 24: 263–272, 2000.
Viidik A. 1993
Functional properties of collagenous tissues.
Int Rev Connect Tiss Res 6: 127–215, 1993
Valentine PJ, Khan KM, Cook JL, et al: 1998
The VISA score: an index of the severity of jumper's knee (patellartendinosis): Victorian Institute of Sport Tendon Study Group.
J Sci Med Sport 1998;1(1):22-28
Health and Fitness Journal. 4(1), 7-16 2000
Waterston SW, Maffulli N, Ewen SWB. 1997
Subcutaneous rupture of the Achilles tendon: basic science and some aspects of clinical practice.
Br J Sports Med 1997; 31: 289–98.
Williams, J. G. 1986
Achilles tendon lesions in sports.
Sport Med. 3:114-135, 1986.
Williams RJ, Attia E, Wickiewicz TL, and Hannafin JA. 2000
The effect of ciprofloxacin on tendon, paratenon and capsular fibroblast metabolism. Am J Sports Med 28: 364–369, 2000.
Williams MAET, Miller GR, and Stauber WT. 2002
Is active force production of skeletal muscles altered by collagen content?
Proc Canadian Biochem Meet Calgary Canada 2002, p. 57.
Yasuda T, Kondo S, Homma T, and Harris RC. 2000
Regulation of extracellular matrix by mechanical loading in rat glomerular mesangial cells.
J Clin Invest 98: 2000