To be successful, an equine athlete needs a functional locomotor system that combines muscular strength and coordination with sufficient tissue resilience to withstand athletic performance.
Most equine lameness results from repetitive strain injuries to the musculoskeletal tissues. Each tissue – bone, articular cartilage, muscle, ligament, and tendon – responds optimally to a specific type of exercise imposed at a specific age. Bone and muscle can be strengthened throughout life, but articular cartilage, ligament and tendon undergo most of their adaptive changes before age 2 and the response to exercise occurs concurrently with changes due to maturation and aging. This talk describes the timelines for optimal tissue adaptation, the appropriate type of exercise to strengthen different tissues, and the reasons for tissue failure.
MECHANOTRANSDUCTION
Tissue adaptation involves the process of mechanotransduction, by which cells convert mechanical stimuli due to locomotion into electrochemical activity within the tissues.
During a workout, microscopic tissue damage occurs and is followed by tissue regeneration during the subsequent 24 to 48 hours. Ideally, the amount and frequency of exercise are balanced to allow sufficient time for tissue repair between workouts. Over time, through repeated cycles of damage and repair, the tissues adapt to the regular workload. Bone and muscle respond to strength training throughout the horse’s lifetime. However, articular cartilage, tendon and ligament are time-limited, being most responsive early in life and showing minimal adaptation after age 2.
Mechanotransduction allows the locomotor tissues to perceive the stimulus of exercise and adapt their strength according to the applied loads:
- Strains within the physiological range maintain the status quo.
- Strains below the physiological range lead to tissue resorption and/or loss of strength.
- Strains above the physiological range promote adaptive changes.
- Excessively high loads cause microdamage and targeted remodeling to replace damaged tissue
BONE
The skeletal framework supports the horse’s weight and provides a system of levers moved by muscular contractions. Since horses are precocial, the skeletal system is already well developed at birth. Prenatal bone development anticipates the needs of the neonate, whereas postnatal development occurs as a reaction to the loading environment.
Bone consists of mineral crystals laid down on collagen fibers, providing a combination of rigidity and strength to resist compression and tension, respectively. Bone adaptation is stimulated by dynamic, but not static, loading. High strains and high strain rates, as in sprinting, are most effective in stimulating bone adaptation. Only a few loading cycles are needed. Tensile and compressive, but not shear strains stimulate adaptation. After bone has adapted to the regular loading regime, it becomes less responsive to these signals, and increased loading is necessary to promote further increases in bone strength.
BONE MODELING:
Increases the diameter of the shaft to maintain a safe level of stress.
- Periosteal osteoblasts lay down new layers of compact bone around the shaft.
- Endosteal osteoclasts remove bone on the internal surface to increase the width of the medullary cavity.
- The bone is strengthened without a large increase in weight that would reduce energetic efficiency.
- Bone modeling occurs only in young horses.
BONE REMODELING
Bone removal precedes new bone formation.
- It takes several months to complete the remodeling cycle.
- There is a period when old bones have been resorbed but new bones have not yet been formed, so the bone is weakened and susceptible to damage.
- Remodeling continues throughout life in response to exercise but it slows with age.
- Bone adapts to withstand the regularly applied loads.1
The amount of stress needed to fracture a bone is greatest in compression, least in shear, and intermediate in tension. Therefore, when a bone is bent, it fractures on the convex (tension) side rather than the concave (compression) side. Efficient bone adaptation reduces the risk of fracture. After adaptation to the regular loading regime, bone becomes less responsive to these signals. Therefore, progressive loading is necessary to continue increasing bone strength.
Fatigue life is the number of loading cycles a bone can sustain before it fails. Initially, bone fails by the formation of fatigue fractures (cracks) that are repaired by remodeling. If the horse continues to work and microdamage accumulates faster than it can be repaired, fatigue fractures coalesce and may form complete fractures.
Reduced loading, for example, long-term immobilization following injury, results in significant bone loss brought about by increased remodeling of trabecular and endosteal bone. If resorption exceeds formation, there is an overall loss of bone tissue.
ARTICULAR CARTILAGE
Articular cartilage provides a smooth gliding surface and acts as a resilient shock absorber that contributes to damping concussive locomotor forces, especially when the horse travels at speed. However, the cartilage layer is only 2 to 5 mm thick, which limits its shock-absorbing contribution. Hyaluronic acid in the synovial fluid provides a low-friction interface for rotational and gliding movements of the joints.
Articular cartilage is arranged in several layers. The integrity of the superficial layer protects the deeper layers from sheer tensile, and compressive forces transmitted across the joint. It is responsible for most of the tissue’s tensile properties. Cartilage lacks vascularity and innervation. Fluid is squeezed out of the cartilage onto the joint surface during weight-bearing and is resorbed when the joint is unloaded. Maintaining the water content of articular cartilage is crucial for its mechanical properties and for the nutrition of the chondrocytes.
At birth, proteoglycans are evenly distributed throughout articular cartilage giving a homogeneous structure, the so-called blank joint. Functional adaptation is time-limited, with most of the adaptive changes occurring because of the foal exercising freely during the first year of life. This results in the development of topographical heterogeneity, with site-specific adaptations of articular cartilage, subchondral bone and mechanical properties.2 It is only during the early months of life that the collagen network of articular cartilage responds to the stimulus of exercise to reduce the risk of developing degenerative joint disease later in life.
Like other tissues, articular cartilage is continuously remodeled by ongoing formation and degradation. The two main constituents of the extracellular matrix, collagen and proteoglycans, turn over very slowly. Proteoglycan turnover rate is several months to several years, and collagen turnover times are even longer, up to 350 years in mature human cartilage. These very slow turnover rates limit the ability of articular cartilage to be repaired after injury. Thus, osteoarthritis has a poor long-term prognosis for healing, however, some cases can be managed successfully.
Complete immobilization of an immature joint has a permanent, deleterious effect on cartilage development. Inactivity in mature horses leads to articular cartilage degradation, so joint motion is important for maintaining normal structure and function throughout life.
Although articular cartilage benefits from an early start to an exercise program, too much exercise in young, skeletally immature (2 to 3-year-old) horses is associated with more cartilage damage than in those trained less strenuously, resulting in collagen microdamage that progresses to cartilage degeneration and osteoarthritis.
Different joint surfaces respond differently to the same training regimen. For example, following a three-month training on grass and sand tracks, the intercarpal joint showed adaptive increases in cartilage thickness at specific sites. On the other hand, the fetlock joints of the same horses developed wear lines, fibrillation, increased water content and fewer cross-links, which may indicate micro damage with loosening of the collagen network. The fetlocks are notoriously susceptible to exercise-induced damage because of experiencing high loading combined with a large range of motion.
TENDONS AND LIGAMENTS
Tendons and ligaments consist of tough bands of dense fibrous connective tissue with linearly arranged collagen fibers that confer resistance to unidirectional tensile stress. Their functions include force transmission, shock absorption and providing proprioceptive input for maintenance of posture and control of local strain magnitude.
Tendons are firmly connected to muscle fibers at the musculotendinous junction and to bone at the enthesis. Tendon strength depends on the number, size and orientation of the collagen fibrils aligned along the long axis of the tendon. Tendons can sustain loads several times body weight during vigorous exercise but have low loading rates during rest. Muscles in the proximal limbs that generate high power and large force have short, broad tendons, whereas muscles that perform more precise movements have longer, thinner tendons.
At the musculotendinous junction, the tendon’s collagen fibers extend into the body of the muscle for a variable distance; greater penetration increases the surface area for anchoring the tendon to the muscle. This is where the muscle and tendon increase in length during growth.
Tendon innervation is almost exclusively sensory, with Golgi organs and other proprioceptors located near the musculotendinous junction.
Tendon attaches to bone through an enthesis, usually marked by a bony tuberosity. The gradual transition from uncalcified tendon fibers through uncalcified fibrocartilage and calcified fibrocartilage into lamellar bone minimizes stress concentrations while facilitating load transfer from the soft, fibrous tendon to bone. Sometimes, a tendon inserts indirectly into a bone by blending with the periosteum, which is anchored to the underlying bone by collagenous Sharpey’s fibers.
The stress-strain curve of a tendon or ligament has four distinct regions:
- Toe region (0-3% strain) represents straightening of the crimp in collagen fibers
- Characterized by having a low slope (small amount of tension causes large elongation).
- Linear elastic region where the collagen fibrils align in parallel and slide past each other as the tendon lengthens and is completely reversible when the tendon is unloaded.
- Plastic deformation under high strain with irreversible dissociation of cross links between collagen fibrils leading to microscopic failure.
- Complete failure occurs at even higher tension with rupture of large tendon bundles.
Most tendon and ligament injuries in athletic horses are repetitive strain injuries related to cyclic loading during locomotion, with the entheses being particularly susceptible. Due to the nature of the tissue, these injuries heal slowly and incompletely.
Two types of tendons are important in locomotion: positional and elastic.
POSITIONAL TENDONS
- Fairly stiff and almost inextensible, they transmit muscle length changes precisely to the bones.
- Collagen fibers are elongated by sliding between the fascicles rather than fiber extension.
- They are injured relatively infrequently.
- The common digital extensor (CDE) and deep digital flexor (DDF) are antagonistic positional tendons that orient the hoof in preparation for ground contact.
ELASTIC TENDONS
Behave like springs – they stretch when loaded in early stance then recoil elastically when unloaded later in stance.
- The stretch-recoil cycle stores and releases energy that reduces the need for muscular effort.
- During trotting, elastic energy storage is particularly effective in the elastic SDFT and suspensory ligament (SL) that undergo a stretch-recoil cycle during stance.
- Long, elastic tendons in the distal limbs allow the large, heavy locomotor muscles to be confined to the proximal limbs.
- Galloping recruits the lumbodorsal fascia for energy conservation during flexion-extension of the lumbosacral joint.
- Since elastic recoil occurs much faster than muscles can shorten, it offers advantages in movements requiring rapid force generation or high power.
Elastic tendons withstand higher strains than positional tendons before experiencing plastic deformation and failure, they have low safety margins and have high injury rates.
In neonates, tendon and ligament fibrils are small with similar diameters, which is described as a unimodal distribution. In areas of tensile loading, such as the mid-metacarpal region, type I tendon fibrils with larger diameters develop with exercise, and the fibril distribution becomes bimodal, with a mixture of large- and small-diameter fibrils. These areas have low levels of cartilage oligomeric matrix protein (COMP) in the neonate, but this increases in response to loading and by age 2, cross-linking of collagen fibrils, fibril size and distribution resemble those of adult horses. COMP levels are correlated with ultimate tensile strength and are higher in areas loaded in tension than in compression.
Tendon maturation is greatly affected by management, especially turnout. Foals raised on full-time turnout undergo a large increase in size of the SDF tendon during the first six months of life, resulting in a 50 percent larger cross-sectional area compared with stabled foals or foals kept in stalls with or without a brief period of high-intensity daily exercise. Pasture-reared foals also show an earlier change to a bimodal distribution of collagen fibril diameters and, by age 1, have similar biomechanical properties to mature horses. The low-level exercise undertaken during turnout has a profound effect on tendon growth and development. Lack of free pasture exercise leads to the development of biomechanically inferior tendons. On the other hand, additional forced exercise more than turnout does not enhance the benefits.
Ageing tendons undergo structural and compositional changes (Thorpe et al., 2014):
- Elastic tendons accumulate micro-damage within the matrix that increases the risk of injury.
- Loading is associated with decreased collagen recoil and energy recovery, and increased hysteresis.
- Collagen fascicles are less resistant to fatigue, withstand fewer cycles to failure, and are predisposed to tendinopathy and enthesis.
- Stress increases more rapidly in the core than in the peripheral parts of the tendon.
These age-related changes may be accelerated by athletic activity and may partially explain why tendon tissue from horses over age 10 is more susceptible to injury due to cyclical loading.
Elastic tendons operate at high stresses and strains, and with low safety margins. Typical peak tensile strains in the forelimb SDFT are 3 percent at the walk, 6 to 8 percent at the trot, and 12 to 16 percent at the gallop. In laboratory testing, this tendon ruptured at 12 to 16 percent strain in Thoroughbreds and 12.5 percent strain in Warmbloods.
Tendon is viscoelastic, so its response to loading varies with the loading rate. At high loading rates, tendons are more brittle and absorb less energy, but they are more effective in supporting large loads. At low loading rates, they are more viscous, so they absorb more energy while undergoing greater elongation at the same load, but at the expense of reduced ability to support large loads.
The elastic modulus may be changed by removal or deposition of matrix to alter the cross-sectional area of a tendon or by modifying the composition of the extracellular matrix. An exercise-induced increase in SDFT diameter in 2-year-old Thoroughbreds (but not Warmbloods) developed larger, but not stronger, tendons. An increase in volume due to higher water content is an exercise-induced response, but not a beneficial one. In elastic tendons, a larger diameter equates to greater stiffness, which reduces their ability to stretch, so increasing the diameter is not beneficial.
Contrary to popular belief, early training can reduce the risk of tendon injury later in life, because young tendons are better able to adapt to exercise. The positional extensor tendons hypertrophy somewhat with sprint exercise, but not to the same degree as the elastic flexor tendons, which respond to exercise until age 2.
Elastic fibers are deposited and organized prior to maturity but cannot be reorganized in adulthood, so mechanical damage or proteolytic degradation of elastic tendons results in irreversible changes to the form and function of the tissue4. Additionally, elastic tendons get weaker with age and fail at a lower strain rate in older horses. By the time the horse is 5 years old, the SDFT has already begun to degenerate, showing changes in crimp angle and collagen levels, with a reduction in total strength. At this stage, exercise accelerates age-related degeneration.
Both people and horses suffer from age-related tendinopathy that shows similar initiation and progression between species. Tendon injuries primarily affect high-strain, energy-storing tendons. In people, the Achilles tendon, and in horses, the SDFT are most often affected. By contrast, the positional tendons, that are exposed to lower strains are seldom injured.
MUSCLE
Muscles are machines for converting chemical energy into mechanical energy, which is then used to move the body and stabilize the joints. Skeletal muscles are under voluntary control, though many movements during normal gait do not require conscious input.
SKELETAL MUSCLES:
- Are about 75% water, 22% protein, 7% lipids and inorganic salts.
- Connective tissue sheets (fascia) surround and separate entire muscles, muscle bundles and individual fibers.
- A muscle fiber is a long slender cell containing fluid sarcoplasm packed with actin and myosin filaments that slide past each other during contraction.
- Fiber types are SO (slow, oxidative), FOG (fast oxidative-glycolytic), and FG (fast glycolytic).
- Glycogen and triglycerides are energy substrates stored in muscle fibers.
- Capillaries adjacent to the fibers supply nutrients and oxygen to and remove waste products from the muscle fibers.
- Motor nerves convey electrical impulses from the central nervous system to the motor end plate from which the signal spreads through the muscle fiber.
- Sensory nerves provide proprioceptive feedback from muscles and tendons.
Muscle develops tension when cross-bridges on the myosin filaments interact with the actin filaments, causing them to slide past one another and shorten the muscle fiber. Cessation of the impulse to contract allows the filaments to slide apart and restore the original length. When a muscle develops tension, individual fibers either contract or don’t contract, but there is no partial contraction.
The amount of tension generated by the muscle depends on the number of fibers stimulated to contract: a greater number of contracting fibers develops more tension. Calcium plays a key role in the actin-myosin interaction, but it must be removed from the sarcoplasm when the contraction ceases to avoid muscle cramping. An increase in speed within a gait involves recruiting more muscle fibers to generate the larger force that is needed to move faster. The recruitment pattern of the muscle fibers is controlled by the nervous system; the same fibers are always active at any gait and speed.
At the walk, only a small percentage of fibers are recruited, predominantly slow oxidative (SO) fibers, which have the lowest threshold of stimulation. At the trot, additional fibers are recruited, mostly from the SO and fast oxidative glycolytic (FOG pool). At a medium-speed trot about 25 to 30 percent of the fibers are active. As speed increases at the canter and gallop, there is a progressive increase in recruitment of anaerobic fibers. At maximal speed, almost all fibers are active, with both the aerobic and anaerobic energy production systems working at full capacity. Muscle contractions are classified as isometric (no length change), concentric (muscle shortens) or eccentric (muscle lengthens).
Eccentric contractions resist a force, usually gravity. During stance, gravity tends to flex the joints, and the extensor muscles work eccentrically to control the amount of flexion. Later in stance, the extensor muscles act concentrically to provide propulsion. Therefore, each stance phase involves an eccentric-concentric cycle in the extensor muscles along with the storage and release of elastic energy in the elastic tendons.
Muscles are responsive to training throughout life.
Regular exercise affects the structure and chemical composition of muscle fibers through changes in stored energy substrates and enzymes used by aerobic and anaerobic metabolism. In general, endurance exercise enhances aerobic capacity but compromises the power and speed of muscle contraction. Sprinting stimulates the glycolytic machinery to enhance power and speed at the expense of aerobic endurance. Thus, conditioning exercises should be sport specific.
REFERENCES
- 1. Smith RKW, Goodship AE. The Effect of Early Training and the Adaptation and Conditioning of Skeletal Tissues. Veterinary Clinics of North America: Equine Practice. 2008;24(1):37-51. doi:10.1016/j.cveq.2007.11.005
- 2. Lewis CW, Williamson AK, Chen AC, et al. Evaluation of subchondral bone mineral density associated with articular cartilage structure and integrity in healthy equine joints with different functional demands. Am J Vet Res. 2005;66(10):1823-1829. doi:10.2460/ajvr.2005.66.1823
- 3. Harrison SM, Whitton RC, Kawcak CE, Stover SM, Pandy MG. Relationship between muscle forces, joint loading and utilization of elastic strain energy in equine locomotion. Journal of Experimental Biology. 2010;213(23):3998-4009. doi:10.1242/jeb.044545
- 4. Patterson-Kane JC, Firth EC. The pathobiology of exercise-induced superficial digital flexor tendon injury in Thoroughbred racehorses. Veterinary Journal. 2009;181(2):79-89. doi:10.1016/j.tvjl.2008.02.009
About the Author
Hilary M. Clayton, BVMS, PhD, DACVSMR, FRCVS
Dr. Hilary Clayton has performed innovative research in the areas of equine biomechanics, lameness, rehabilitation, athletic conditioning, and the interactions between rider, tack and horse. Based on her studies, she has published 8 books, several hundred scientific papers and many articles in equestrian publications. She was the first incumbent of the Mary Anne McPhail Dressage Chair in Equine Sports Medicine at Michigan State University where she developed and managed a state-of-the-art research facility. Since retiring from academia in 2014, she has continued to perform collaborative research and to make her research results accessible to equine professionals to benefit their daily practice.