Competition, regardless of discipline, exposes the modern equine athlete to injury. Due to the popularity and high profile of equestrian sport, in particular horseracing, accidents are widely broadcast and can have a significant negative impact on public perception and prove detrimental to the equine industry. Reducing the risk of harm is paramount, primarily for the welfare of the horse but also to promote participation and its associated financial benefits. The main aims of training programmes are to condition against, or postpone potential damage for as long as possible, thus increasing the longevity of the horses' career and health. Intrinsic factors such as genetics, apparent externally via conformation and physiological performance, must be considered when evaluating injury potential. Numerous extrinsic factors have been suggested as contributors towards increased injury prevalence in the horse including surface/going (Williams et al, 2001), terrain and its undulations (Singer et al, 2008), number of jumping efforts (Pinchbeck et al, 2004a), jumping downhill obstacles and water jumps (Singer et al, 2008), speed (Pinchbeck et al, 2004a), distance of the competitive test (Parkin et al, 2004a), farriery (Pinchbeck et al, 2004a), and rider and performance demands specifi-cally galloping, jumping and collection (Dyson, 2002). The impact of core parameters such as nutritional status, fitness and the subsequent fatigue that ensues, or the undetected presence of subclinical injury, should also be assessed when examining injury risk.
The anatomical location of tendon injuries varies with specific disciplines (Dyson, 2002; Murray et al, 2010) but all sports horses are susceptible, with a 11–30% incidence of injury reported (Patterson-Kane and Firth, 2009). The superficial digital flexor tendon (SDFT) is the most commonly injured tendon (Cohen et al, 1997) and a higher susceptibility for injury occurs in disciplines which involve galloping and jumping. Tendon injuries in racehorses vary between race type: a 46% tendon injury prevalence has been reported in fat racehorses (Williams et al, 2001; Ely et al, 2004) which increases to 53% in National Hunt horses, where the test combines galloping and jumping (Pinchbeck et al, 2004a, b and c). Show jumpers are prone to tendonitis in the forelimb SDFT and deep digital flexor tendon (DDFT) attributed to the increased loads due to hyper-extension in the meta-carpophalangeal joint when landing from a jump (Dyson, 2002). Event horses are at a higher risk of SDFT injury than horses competing in show jumping and dressage (Murray et al, 2010) with a 17% incidence of SDFT injuries recorded in eventing competition, which increases to a 43.4% incidence rate during training (Singer et al, 2008) due to the requirement for galloping during both. Dressage horses have a reduced presentation of SDFT and DDFT injuries but are prone to suspensory ligament (SL) pathology, the DDFT and SL are closely connected in the distal limb and oedema in the DDFT sheath can restrict SL function. The transfer of the dressage horse's centre of gravity caudally during collection also places increased strains on the hindlimb and a higher presentation of tenosynovitis in the digital flexor tendon sheath has been observed (Dyson, 2002). The majority of tendon injuries occur in the forelimb (97–99%), and of this 73–93% occur in the SDFT (Thorpe et al, 2010). The high incidence of SDFT injury suggests many equine athletes in training may have unknown subclinical pathology present in the tendon and yet be asymptomatic. The ability of the veterinary team to communicate and advise sports horse owners on the relevant risk factors and strategies for prevention of tendonitis is a useful asset. This reviews aims to describe SDFT normal anatomy and physiology, evaluate common risk factors and their contribution to SDFT pathology to propose prophylactic strategies to reduce injury.
Tendon anatomy and physiology
Tendons are composed of a dense fibrous extracellular matrix, mainly consisting of type I collagen, which is synthesized by tenocytes (Thorpe et al, 2010). The collagen is subject to an organizational hierarchy comprising bundles of longitudinally orientated collagen fibrils which systemize to form collagen fi-bres; the fibres incorporate crimp and angulation to facilitate plasticity during locomotion and are interspersed with tenocytes, all of which are surrounded by a protective sheath, the fascicle (Patterson-Kane and Firth, 2009). The fascicles then combine to comprise the functional tendon unit (Stromberg, 1997) (Figure 1). Tendons require high tensile strength and a degree of flexibility; strength is provided by inter-molecular chemical cross links between the collagen fibres (Avery et al, 2005). Fibrogenesis is thought to be coordinated by proteoglycans found in the matrix and facilitates the production of glycosaminoglycan side chains which ‘hold’ the fibrils apart in an organ-ized manner and aid strain distribution (Thorpe et al, 2010). Glycoproteins, primarily collagen oligomeric matrix protein (COMP), are thought to facilitate fi-brillogenesis and therefore have a central role in the repair of microlesions in the tendon fbrils (Smith et al, 2000). Tenocytes can synthesize collagen, prote-oglycans and enzymes, specifically matrix metallo-proteins, which play a key role in degradation of scar tissue during remodelling.
Tendon function
Tendons join muscle to bone and their role is to stabilize the limbs and joints during flexion and extension, or to position the limbs during locomotion. Tendon tissue can also act as an energy store during locomotion, primarily the SDFT, with the ability to convert potential energy to kinetic energy during recoil in the swing phase of each stride to reduce the energetic cost of locomotion (Thorpe et al, 2010). Therefore tendon functionality is critical to the attainment of optimum performance in the sports horse. Research has iden-tified that galloping and jumping in particular place large loads or strains on tendon units in the distal limb (Williams et al, 2001; Pinchbeck et al, 2004a; Thorpe et al, 2010). During galloping the horse's centre of gravity moves cranially, its head and neck extend and lower to place 60% of the bodyweight onto the forehand thus creating increased load (represented as strain) through the forelimbs. Stephens et al (1989) found in vivo strains (actual galloping) of 16% in the SDFT which correspond to in vitro strain (cadaver models) levels of 15–17% (Dowling et al, 2002). To put this in context, failure of tendon integrity resulting in microdamage has been recorded at strain levels of 12– 18% which correspond to the strain levels found during galloping (Goodship and Birch, 2001). Jumping also increases the strain on both the SDFT and DDFT tendons. During take of and landing these tendons are stretched in correspondence to flexion and extension of the metocarpophalangeal and metotar-sophalangeal joints respectively. The increased load can result in microdamage and excessive stretching can rupture tendon fibrils. Disciplines which require horses to regularly undertake gallop or jump exercise, in training or competition, will enhance the risk of tendon microdamage and prophylactic strategies to ascertain impact of exercise on the tendon and identify subclinical pathology are warranted to enhance welfare and optimize performance.
Tendon plasticity and deformation during locomotion can be illustrated using a stress–strain curve (Figure 2). Flexibility in tendon anatomy is provided via the crimp arrangement of the fibrils, as the tendon stretches the crimp ‘straightens’ lengthening the functional unit of the tendon (Goodship and Birch, 2001). However, this is limited and if overstretched, deformation and damage occurs to the fibril. Dowling and Dart (2005) found that SDFT has variable tensile strength in different regions, therefore it should be remembered that the tendon is a dynamic functioning unit; each fibril will have its own stress–strain properties and may fail at a slightly different level to its neighbour. The cross-sectional area of the tendon is inversely proportional to collagen content and tensile strength, therefore injured tendons also present with an increased cross-sectional area on examination (Dowling and Dart, 2005). A horse may present sound and have accumulated subclinical tendon pathology, the effects of cumulative microdamage and risk factors, for example the influence of shoeing on distal limb loading, will contribute to which fibrils fail and if a catastrophic injury or minor tendonitis will present.
Tendon pathology
Wilson and Goodship (1994) discovered, during postmortem examination, that tendons when stretched to rupture display characteristic patterns of failure with the central fibres failing first. The work suggested that the core of the tendon undergoes degeneration predisposing it to subsequent breakdown. Fibril disruption is accompanied by haemorrhage and formation of intra-tendinous haematomas which manifest as oedema and heat, due to the increased blood flow in response to the inflammation, in the tendon sheath and surrounding tissues. Rupture of fibres may cause further swelling; if large numbers of adjacent fibres rupture this can lead to core lesions between the remaining fibres. Build up of inflammatory fluids between fibres and within core lesions exert pressure on the remaining fibres, damaging them and exacerbating the problem. If the integrity of the tendon unit is disrupted and exercise is continued, then complete rupture may occur. The pathological changes produce discolouration in the damaged area and produce changes in the composition of the extracellular matrix, increased glycosaminoglygans, type III collagen and matrix metalloproteases (Thorpe et al, 2010).
Following rupture, cellular proliferation, remodelling and maturation occurs within the tendon fibrils (Patterson-Kane and Firth, 2009). During the proliferation stage small blood vessels invade the area while fibroblasts migrate to the damaged area to produce collagen. Fibrils are repaired, but the type III collagen produced is laid down in a haphazard pattern disrupting the organizational hierarchy of the tendon (Thorpe et al, 2010). Maturation crimp enables crimp organization to be partially re-established, as fibril diameter increases with stable chemical cross links. Remodelling is a lengthy process taking weeks to months and characterized by scar tissue formation and adaptation in the tendon to new loading patterns (Wilson and Goodship, 1994). Ultrasound scanning is valuable in determining the stage of remodelling, to establish when longitudinal alignment of the tendon fibres has occurred, in order to inform rehabilitation management (Smith et al, 1994). Remodelling does not necessarily reconstitute normal structure and function, resulting in permanent scar tissue within and between fascicles (Patterson-Kane and Firth, 2009). Scar tissue is inelastic and the repaired tendon is therefore predisposed to recurrent damage (Thorpe et al, 2010).
Factors that contribute to tendon pathology
Risk factors can be divided into two main categories: intrinsic and extrinsic. Studies have shown that with intrinsic factors such as increasing age, the injury risk factor increases (Williams et al, 2001) with significant associations between the age of horse and the rate of tendon and ligament injury recorded (Ely et al, 2004). Interestingly, gender does not seem to have an effect on tendon injury rates with damage more commonly attributed to the impact of repetitive strain (Ely et al, 2009). The conformation of the hoof, particularly a reduced hoof pastern axis characterized by long feet and low heels (Pinchbeck et al, 2004a), an increased angle of the metacarpophalangeal joint (fetlock joint) and carpus valgus, and outward angulation of the knee, have all been shown to predispose the horse to SDFT injury as these conformational defects place the flexor tendons, especially the SDFT, under more strain (Weller et al, 2006).
Training requirements and discipline impact on risk of tendon injury, and any exercise which increases loading in the distal limb, or continuing with the current level of training when subclinical pathology exists, will enhance the risk of damage. Remember, the SDFT experiences strain levels of approximately 16% during galloping and rupture of the tendon has been documented at levels between 12–20% (Smith and Goodship, 2008). Horses gallop at 120% efficiency with the additional 20% energy reserve in the SDFT, the tendon should act like a ‘spring’ to release this ‘extra energy’ (Marlin and Nankervis, 2002). Cumulative microlesions will reduce ‘spring’ and potentially lower the strain load at which deformation of the tendon occurs. Tendons do not just snap. Lesions are frequently preceded by degenerative changes in the extracellular matrix. Tendon injury can occur either as a result of a single catastrophic overload period or due to microdamage accumulation which increases every time the limb is loaded, and is not allowed to repair prior to reloading, and eventually leads to failure of the tendon fibres (Wilson and Goodship, 1994). During exercise muscle recruitment should act to decrease the stress/load on the tendon, but when the muscle fatigues, vibration in the musculo-tendi-nous unit transfers an increased load onto the tendon fibrils. Therefore, when the tendon is put at risk of increased strain via galloping, jumping or continuing to exercise during fatigue, tearing and microdamage to the tendon fibrils occurs and injury ensues.
Tendonitis is most commonly associated with excessive stress however there are other reasons for its occurrence. The cyclical loading of tendons during locomotion generates energy for movement but also heat as a by-product. Hysteresis, the measure of energy during cyclical loading, has been measured in the tendon core at 43–45°C (Patterson-Kane and Firth, 2009). The equine distal limb has a relatively poor blood supply and is inefficient at dissipating heat, it is suggested that the local thermal effects may result in death or impaired metabolism of tenocytes which is detrimental to tendon repair (Dowling and Dart, 2005). Localized ischaemia can also occur as a result of cyclical loading in the tendon which may be painful and impact on cellular metabolism but detrimentally stimulates the production of super oxides during reperfusion; super oxides are toxic to tissue and can damage tenocytes and thus the tendon matrix.
Extrinsic factors can impact on tendon injury prevalence primarily via contribution to increased loading in the distal limb or repetitive strain progressing cumulative microdamage in the tendon. Competition surfaces exhibit variable traction, friction and stability properties which can lead to slipping, falling and increased strain on tendons. A poor quality surface, deep or heavy going surface or terrain which is undulating can lead to hyperflexion in the fetlock joint, or slipping, and this can increase the load in the tendon (Pinchbeck et al, 2004a,b and c; Ely et al, 2009). Disciplines which require sharp turns or abrupt stopping will also place more strain in the tendons in the distal limb. Jumping, particularly in sports such as eventing, will enhance injury risk as landing will produce hyperflexion in the fetlock with the loading force of the horse's bodyweight and gravity applied to the SDFT tendon plus it may be performed on a downhill gradient which will increase the stress the tendon unit is placed under. Fatigue results in a reduction in stability of the musculoskeletal system of the horse and therefore can apply increased load on the soft tissue structures in the distal limb to produce effec-tive locomotion. It should not be surprising therefore that SDFT injury risk is raised for increased distances, number of jumping efforts and when the surface is heavy or deep (Williams et al, 2001; Pinchbeck et al, 2004a). Older horses also exhibit a higher risk of tendon injury probably due to the accumulated damage of years of repetitive strain in the distal limb (Parkin et al, 2004a). Intensity of training regimens are predominantly decided by the trainer, and this is supported via research findings where fracture, tendon and ligament injury incidence rates have been found to vary significantly between trainers (Ely et al, 2009). Training intensity affects the injury and fatality rates both while training and during competition, and could be the accumulation of repetitive strain injury. Additionally, an association has been recorded between injury rates and different yards, not just between trainers, potentially showing that additional management factors could also influence outcome (Ely et al, 2004). For example, correct farriery and regular shoeing (5–6 week interval) are vital in reducing the risk of injury and placing unnecessary strain on musculoskeletal structures including the tendon (Pinchbeck et al, 2004a).
Strategies for injury prevention
Tendon injury can have dire consequences for the sports horse; therefore prevention is key to prolonging career and optimizing performance. Evaluation of underlying pathology and recognition by the rider that the horse's performance has deteriorated or changed may provide an indication that a tendon has been compromised. However many amateur riders may not have the skill to perceive minor adaptations within their mount (Dyson, 2002) and generic training strategies and increased veterinary intervention may provide more successful prophylaxis.
Management
Injury prevention is advantageous because post injury the musculoskeletal system is compromised and even after treatment and rehabilitation, the capacity of the damaged area and supporting structures will be reduced (Smith and Webbon, 2005). During rehabilitation the contralateral limb to that injured will also have had to cope with increased loading and the resultant adaptation in soft tissue will need to be addressed to reduce injury potential. Prevention is a more effective strategy especially in disciplines where galloping and jumping are integral as a slight reduction in a tendon's capacity to stretch and recoil could reduce performance. Simple research justified pre-ventative strategies include the modification of training schedules. Galloping a minimum of 805–2012 m (4–10 furlongs) per week and the avoidance of sand or woodchip gallops have been shown to reduce the risk of injury (Parkin et al, 2004a and b). Regular farriery should occur to correct poor foot conformation to reduce loading on the SDFT and DDFT, and planning when shoeing occurs within the competition schedule should take place as evidence suggests that horses shod in excess of 1 week prior to racing exhibit a greater risk of tendon injury compared within those shod within the previous week (Pinchbeck et al, 2004a). An increased vigilance on the behalf of the ground staff and pre-competition committees, may avoid the incidence of musculoskeletal injury through closer monitoring of the track moisture content to avoid excessively hard ground, which would result in increased strain and loading in the distal limb, and could be combined with implementation of more rigorous pre-competition lameness checks (Bailey et al, 1998). More research is required to evaluate the type and size of ‘risk fences’ particularly downhill fences to adapt these to avoid excessive risk of tendon injury while not affecting the quality of competition.
Subclinical evaluation
Subclinical evaluation methods aim to assess tissue integrity and detect pathological changes prior to clinical symptoms reducing injury occurrence, time spent in convalescence and treatment cost. The development of a specific assay for a molecular marker for tendon injury would be an efficient subclinical detection strategy (Smith and Goodship, 2008). COMP is a protein the fragmentation of which is consistent with tendon injury and identification. This assay has already been shown to detect tendon damage or sepsis within the tendon sheath (Smith and Heine-gard, 2000). Further work is required to develop the sensitivity of this assay for detection via circulating blood which would be advantageous to the efficacy of diagnosis. Another proposed method of detecting subclinical damage to a tendon is to undertake prophylactic monitoring of the cross-sectional area of tendons, especially the SDFT, ultrasonographically at regular intervals. An increase in cross-sectional area is indicative of the inability of the tendon to cope with the current workload (Dowling and Dart, 2005) and off-incidence ultrasonography is showing potential to assess tendon scar tissue as an emerging technique (Chatham, unpublished data). These methodologies could enable workload to be moderated with respect to tendon anatomy and pathology to prevent injury occurrence, or used during rehabilitation post treatment to assist in an ascending exercise regimen avoiding an injury relapse.
Treatment and return to competition
Pain from inflammation associated with tendoni-tis may not present as lameness until it exceeds the horse's tolerance level or results in anatomical dysfunction (King and Mansmann, 2005). A clinical lameness workup and a veterinary diagnosis (including ultrasonography) should occur, and a treatment and rehabilitation programme should commence. Treatment for most tendon injuries involves a multi-disciplinary approach; it is important to ensure all professional persons involved understand the cause, diagnosis and treatment of the injury to maximize the possibility of return to competition (King and Mans-mann, 2005). The aim of treatment is primarily not to cause further damage and secondly for the horse to stay in training, if appropriate, not to reinjure the tendon and to return to the prior level of performance. The derived treatment and rehabilitation programme either leads to recovery or if unsuccessful results in prolonged chronic injury. There are three phases to tendon healing: acute inflammation and demarcation (~10–14 days post-injury); proliferation; and remodelling of the tendon matrix. During the inflam-mation and demarcation phase the disrupted tendon fibres are digested by proteolytic enzymes via phago-cystosis resulting in an enlarged lesion (and the classical representation of tendon injury: oedema). The size and extent of the initial injury is related to the successful return to competition (Figure 3); the larger the lesion, the more guarded the prognosis. Generally horses will require 9 months to recover from strain-induced SDFT injury but this may be extended to 18 months in some cases (O’Meara et al, 2010).
The aim of treatment is to restore functionality but also to prevent enlargement of the lesion; treatments advocated include restriction of exercise often ac-companied by non-steroidal anti-inflammatory drugs (NSAIDs) to inhibit inflammation, and reduction of loading on the tendon. This can take the form of box rest or reduced exercise intensity and frequency for tenosynovitis. Therapeutic interventions such as cryotherapy, hydrotherapy, magnetic field therapies, LASER, ultrasound therapy are employed within conservative rehabilitation programmes with variable success (Buchner and Schildboeck, 2006). More radical treatments include pin or bar firing, superior check ligament desmotomy, introduction of insulinlike growth factor 1 and emerging regenerative technologies such as stem cells and platelet rich plasma (Guest et al, 2010). Stem cells retain the capacity to differentiate into new cells and matrix types and therefore in tendon healing should promote production of type 1 collagen which will organize into the original hierarchal structure without scar tissue formation. Currently, stem cell therapy is most successful using bone marrow mesenchymal progenitor cells; in National Hunt racehorses an ~30% re-injury rate has been recorded from horses treated with stem cells and that returned to full training during a 2 year follow-up period, which is a significant improvement on conventional therapies (56% re-injury) (Guest et al, 2010).
Another limiting factor to healing is considered to be the avascular nature of the tendon. Autologous platelet rich plasma administered directly into the tendon introduces a range of growth factors including insulinlike growth factor-1, which facilitate healing and has recorded similar success rates to stem cell treatments (return to racing) post tendon injury in racehorses (~27%) (des Moset al, 2008). However return to competition as an indicator of success should be interpreted with caution. O’Meara et al (2010) recorded a 53% re-injury rate post SDFT tendonitis in racing thoroughbreds of 42% that made a successful return to competition. However, of the horses that returned to racing only 34% managed three races and 22% five races demonstrating that tendon injury is often career limiting. When a horse is suffering from chronic injury, the ethical implications and the welfare of the horse must be paramount in deciding the clinical intervention and it may lead to euthanasia. Horses that do recover from an injury often do return to competition and of those that do, the majority compete at a lower level than that prior to injury (Dyson, 2004) therefore a change of career may be a viable treatment and ethical option.
Conclusion
All equestrian sports have associated risks with the potential to result in injury and fatality to both horse and rider. Tendon injuries and specifically SDFT ten-donitis is a major contributing factor to musculoskel-etal injury and wastage of equine athletes. Through biological advances and research development more effective treatment methods are becoming available which promote higher rates of return to performance post tendon injury. Although improving treatment is advantageous, the key to significantly reducing the injury rate is through prevention and the utilization of research to inform training strategies. Increasing the health and longevity of the sports horse will enable the equine industry to retain owners, increase participation and boost the public profile which hopefully will bring economic benefits as well as improving the welfare of the equine athlete.