Recent Lower Limb Research from the McPhail Center Hilary M. Clayton, BVMS, PhD, MRCVS Mary Anne McPhail Dressage Chair in Equine Sports Medicine College of Veterinary Medicine Michigan State University East Lansing, MI 48854 This presentation describes some general aspect of limb function with particular reference to hoof movements and function. The research upon which this presentation is based was performed at the trot, unless stated otherwise. During every stride, each limb has a stance phase when it is in contact with the ground and a swing phase when it is moving through the air. Traumatic insults usually occur during the stance phase when large forces are imposed on the limb. However, the swing phase affects the aesthetic quality of the gaits and tends to capture the eye of the observer. Stance Phase The stance phase is the period from ground contact to lift off. It can be divided into four phases: initial ground contact, impact phase, loading phase, and breakover. Initial Ground Contact When viewed from the side, hoof contact with the ground is classified as heel first, flat footed or toe first. The manner of contact is influenced by gait, speed, farriery, and lameness. The hind limbs show a greater tendency to heel first contacts than the forelimbs. Heel first contacts are exaggerated during high-speed locomotion (figure 1) and when horses are trimmed with an upright hoof angle. The frequency of toe first contacts increases when the hoof is trimmed with an acute angle (Clayton 1990). For movements in which the hoof approaches the ground with a vertical trajectory, such as piaffe, toe first contacts are normal (figure 1). With certain types of lameness a characteristic manner of hoof contact occurs as a means of reducing pain by shifting the loading away from the affected structures. The toe first contacts of horses with navicular disease are a familiar example. The manner of initial ground contact is likely to affect the forces and accelerations applied to the limb during the subsequent impact phase, though limited information is available on this topic. Figure 1: Toe first contacts occur when the limb approaches the ground with a vertical trajectory (left), whereas heel first contacts are exaggerated at high speed (right). Sinking of the fetlock at midstance reflects the magnitude of the vertical ground reaction force in the weight-bearing limb. Impact Phase When the hoof contacts the ground it is moving forward and downward. It is brought to rest during the impact phase, which occupies the first 50 milliseconds (1/20 second) after ground contact. During this time the limb undergoes rapid deceleration that causes a shock wave to travel up the horse’s limb. The shock wave has high amplitude and rapid vibration frequency that are potentially damaging to the bones and joints. The majority of injuries to the locomotor system occur not as a result of a single catastrophic incident but as a consequence of the cumulative damage that occurs from the many strides taken during training and competition. Impact is the most damaging phase of the stride for the bones and joints. Factors that affect the amplitude and frequency of impact shock include speed, surface and farriery. Faster speeds are associated with higher impact shock, and this is why racehorses often develop fatigue fractures or bone sclerosis, that precede complete fractures. A more chronic impact-related problem is degenerative joint disease, which is the most common reason for premature retirement of sport horses. The repeated traumatic effect of impact shock during years of training and competing is a primary factor in the development of degenerative joint disease, but the effects do not become apparent until permanent damage is present and the horse becomes lame. Therefore, trainers must make every effort to reduce the effect of impact shock throughout the horse’s career by working on good surfaces and optimizing hoof balance and shoeing. Studies using accelerometers attached to the hoof wall have shown extremely high decelerations and forces associated with impact, which are measured in terms of ‘g’ forces. The hooves of trotting horses may experience deceleration of the order of 100 g on hard ground. The hooves of racehorses galloping at racing speed are subjected to hoof decelerations greater than 400 g (Nunamaker, personal communication). Impact deceleration and shock are higher when horses are shod with steel shoes than when they are barefoot, but certain shoes and shoe/pad combinations are associated with lower impact shock at the level of the hoof wall in exercising horses (Benoit et al., 1993). Studies in cadavers (Lanovaz et al., 1999) did not find an increase in impact shock in the phalanges with the use of steel shoes, suggesting that the soft tissues within the hoof, such as the laminae and the digital cushion, may filter out some of the high frequency vibrations. Willemen et al. (1997) reported a similar effect in live horses. Undoubtedly, impact shock is an important cause of lameness and the farrier plays a crucial role in avoiding excess impact shock due to unbalanced ground contact. More research is needed to further our understanding of the effects of hoof balance and shoeing on impact shock. Further testing will be necessary as new materials and products become available. Loading Phase Loading and unloading occupy the period from the end of the impact phase until breakover. During this phase forces are applied more gradually than during impact and without rapid vibrations. In trotting horses, the vertical force peaks at midstance, after which there is a period of unloading. The longitudinal force retards the horse’s forward motion during the loading phase and provides forward propulsion during unloading. Midstance occurs when the cannon bone is vertical, which corresponds with the time when the fetlock joint is maximally extended and the vertical force reaches its peak value. The amount of fetlock joint extension is proportional to the magnitude of the peak vertical force (figure 1). After midstance the vertical force declines steadily until the hoof leaves the ground. At the same time the fetlock joint rises and flexes. During the unloading phase, tension in the flexor tendons and the SL is reduced, and they start to recoil elastically. The release of elastic energy helps to flex the distal joints after lift off. The longitudinal force is propulsive during the unloading phase. Weight-bearing lamenesses are associated with a head nod (the head is raised as the lame forelimb is bearing weight or lowered as the lame hind limb is bearing weight) and the lack of a suspension (airborne phase) following the stance phase of the lame limb (Buchner et al., 1996b). Decreased loading of the lame limb results in reduced flexion of the coffin joint and reduced extension of the fetlock. The more proximal joints may act as load dampers with the shoulder or hock showing increased flexion as a means of reducing the peak forces in the lame limb (Buchner et al., 1996a). Lame horses also tend to have a longer stance duration in the lame limb, which has been interpreted as a means of reducing the peak vertical force by distributing the total load over a longer period of time (Buchner et al., 1996a). Breakover Breakover begins when the heels leave the ground and start to rotate around the toe of the hoof, which is still in contact with the ground. Breakover is initiated by tension in the distal check ligament (DCL) acting through the deep digital flexor tendon (DDFT), combined with tension in the navicular ligaments. On a hard surface, the hoof remains flat on the ground until heel off. On a softer surface the toe rotates into the surface prior to heel off which reduces tension in the DCL-DDFT and navicular ligaments. This, in turn, reduces pressure in the navicular region. Therefore, a surface that allows the toe to dig in during push off is usually beneficial in horses with navicular syndrome or other types of caudal heel pain. Toe off is the instant at which the toe leaves the ground. After lift off, the elastic tendons and ligaments, that were stretched during the loading phase, recoil in an unrestrained manner. The initiation of breakover is an important part of the stride, especially in horses with caudal heel pain. Studies of the effects of different shoe types (rolled toe, square toe, rocker toe) did not reduce the duration of breakover in horses trotting on a hard surface (Clayton et al., 1991; Willemen et al., 1996). An acute hoof angulation has been shown to prolong the duration of breakover (Clayton 1990), presumably due to a slower rotation of the hoof segment though the angular velocity was not actually measured. Raising the heel by 6o delayed the onset of breakover, but the forces required to initiate breakover were reduced (Clayton et al., 2000) Swing Phase In the swing phase the limb is initially protracted (pulled forward) then, in the final part of the swing phase, it is retracted (pulled backwards) prior to initial ground contact. The purpose of this "swing phase retraction" is to reduce the horizontal velocity between the hoof and ground at initial ground contact. The swing phase retraction has a longer duration in the forelimbs than in the hind limbs, and this explains why the horizontal velocity is lower in the forelimb than the hind limb at ground contact. In general, the faster the trotting velocity, the higher the hoof velocity at impact. This results in higher impact forces at faster velocities (Clayton, unpublished). During the swing phase the limbs act in a pendulum-like manner. The forelimb rotates with its pivot point in the upper part of the scapula (figure 2). Since horses do not have a clavicle or a shoulder girdle, the whole scapula is free to rotate back and forth on the side of the chest wall. The hind limb rotates around the hip joint in the walk and trot and around the lumbosacral joint (just in front of the croup) in the canter and gallop (figure *). The lumbosacral joint is the only part of the vertebral column from the base of the neck to the tail that allows a significant amount of flexion (rounding) and extension (hollowing) of the back. At all the other vertebral joints the amount of motion is much smaller. Moving the point of rotation from the hip joint to the lumbosacral joint increases the effective length of the hind limbs and, therefore, increases the stride length. Figure 2: Rotation points for the fore and hind limbs in symmetrical gaits, such as walk, trot and pace (left) and asymmetrical gaits, such as canter and gallop (right). Movements of the entire limb are due to contraction of powerful muscles in the upper limbs, with the distal limbs following passively, that is without active muscular contraction, as a result of inertial forces. When the hoof leaves the ground, elastic recoil of the flexor tendons and suspensory ligament raises the hoof, pastern and cannon to initiate flexion of the distal joints. Limb flexion during swing makes an important contribution to reducing the moment of inertia and facilitating the forward swing of the limb. The horse has evolved with the heavy tissues in the proximal limb, while the distal limb is very light in weight; from the carpus or tarsus distally, the limb accounts for less than 1% body weight. Therefore, the weight of the shoe has a large effect on energy expenditure. This is an important consideration in endurance sports. Heavy shoes impart greater momentum to the limb during the swing phase and carry the risk of loss of control of limb retraction in preparation for ground contact. Balch et al. (1996) investigated the effect of doubling the weight of the shoe. The results showed no effect on stride length, stride duration, or breakover. There was an increase the maximal heights of the hoof, fetlock and carpus during the swing phase and the peak height of the flight arc tended to occur later in the swing phase. Also, the hoof and pastern segments had a more acute angle at ground contact, which probably reflected the loss of control over the terminal swing phase. Thus, the heavier shoes required greater energy expenditure to overcome inertia both at the start and end of the swing phase. The elbow flexors work harder to overcome inertia and initiate protraction of the forelimb when shoe weight is increased and the albow extensors work harder to control the forward momentum and retract the limb in preparation for ground contact (Singleton et al., 2003). A study using toe weights in Standardbred trotters (Willemen et al., 1994) also found an elevation of the flight arc with extra weight. Interestingly, poor movers that had insufficient limb folding and carpal elevation showed an improvement in gait with the toe weights, whereas good movers showed little, if any, change in limb kinematics when toe weights were used. Fore Hoof Kinematics in Swing In the forelimbs, the elbow muscles drive the limb movements. The elbow flexors are active in early swing to flex the elbow and initiate limb protraction. The elbow extensors become active in the later part of swing to slow the forward movement of the limb and initiate elbow extension and limb retraction. As the limb is protracted in early swing, the fore hoof is accelerated forward and upward reaching its highest position at about 40% swing (figure 3). Maximal height of the hoof increases with velocity. For example, the typical Thoroughbred raises the hoof to a height of about 8 cm when trotting slowly (2 m/s) and 18 cm when trotting faster (5 m/s). This shortens the length of the limb and decreases its moment of inertia, which makes it easier to protract the limb. The mechanism by which the hoof is raised higher involves more flexion of the elbow to raise the forearm combined with greater flexion of the carpal joint. After reaching the peak of its flight arc, the hoof is lowered as the lower limb swings through. The hoof is at its lowest around 70% swing, when ground clearance is as little as 1-2 cm in some horses, indicating that precise coordination is needed to avoid stumbling. A second elevation of the hoof then occurs as the distal limb is reoriented in preparation for ground contact. The height of this second hoof elevation does not appear to change with velocity, but it does show a lot of variation between individual horses. Those that have a ‘daisy cutter’ stride show only a little elevation of the hoof in late swing, whereas those that have a more animated gait show much more elevation. The fore hoof reaches peak forward velocity, which is approximately double the horse’s forward velocity, around 70% swing (figure 4). Forward velocity of the hoof is then reduced as the limb is retracted in preparation for ground contact. Hind Hoof Kinematics in Swing In the hind limbs, the hip muscles drive protraction and retraction of the entire limb, while the hock muscles raise and lower the distal limb to ensure that the hoof clears the ground. In early swing the hip flexors contract to flex the hip and initiate limb protraction, and the hock flexors contract to flex the hock and raise the distal limb. In late swing, the hip extensors slow flexion and initiate extension of the hip, which retracts the entire limb. The hock extensors initiate hock extension as the hoof reaches toward the ground. As the hind limb is protracted, the hoof accelerates forward and upward, reaching its highest point around 20% swing (figure 3), which is considerably earlier than in the fore hoof (40% swing). The peak of the flight arc increases with speed, but is generally lower in the hind hoof than in the front hoof. The hind hoof is lowered as the limb swings through, with the toe reaching its lowest point before the middle of the swing phase. A second elevation, the height of which does not vary with speed, occupies the second half of swing. The second elevation is lower than the first. The hind hoof reaches its peak forward velocity around 40% swing (figure 4), which is considerably earlier than in the forelimb (70% swing). Figure 3: Trajectories of the hind hoof (dark line) and fore hoof (gray line) during the swing phase of the stride in a horse trotting at * m/s. Figure 4: Forward velocities of the hind hoof (dark line) and fore hoof (gray line) during the swing phase of the stride in a horse trotting at * m/s. References Balch, O. K., Clayton, H. M., & Lanovaz, J. L. (1996). Weight- and length-induced changes in limb kinematics in trotting horses. Proc Am Assoc Equine Pract, 42, 218-219. Benoit, P., Barrey, E., Regnault, J. C., & Brochet, J. L. (1993). Comparison of the damping effect of different shoeing by the measurement of hoof acceleration. Acta Anat, 146(2-3), 109-113. Bushe, T., Turner, T. A., Poulos, P. W., & Harwell, N. M. (1988). The effect of hoof angle on coffin, pastern and fetlock joint angles. Proc Am Assoc Equine Practnr, 33, 729-738. Buchner, H. H. F., Savelberg, H. H. C. M., Schamhardt, H. C., & Barneveld, A. (1996a). Limb movement adaptation in horses with experimentally induced fore- or hindlimb lameness. Equine Vet J, 28(1), 63-70. Buchner, H. H. F., Savelberg, H. H. C. M., Schamhardt, H. C., & Barneveld, A. (1996b). Head and trunk movement adaptations in horses with experimentally induced fore- or hindlimb lameness. Equine Vet J, 28(1), 71-76. Clayton, H. M. (1988). Comparison of the stride of trotting horses trimmed with a normal and a broken-back hoof axis. Proc Ann Conv Am Assoc Equine Practnr, 33, 289-298. Clayton, H. M. (1990). The effect of an acute hoof angulation on the stride kinematics of trotting horses. Equine Vet J, Exerc Physiol Suppl, 86-90. Clayton, H. M., Sigafoos, R., & Curle, R. D. (1991). Effect of three shoe types on the duration of breakover in sound trotting horses. J Equine Vet Sci, 11(2), 129-132. Clayton, H.M., Willemen, M.L., Lanovaz, J.L. and Schamhardt, H.C. (2000) Effects of a heel wedge in horse with superficial digital flexor tendinitis. Vet. Compar. Orthop. Traum. (in press). Lanovaz, J.L., Clayton, H.M., Colborne, G.R. and Schamhardt, H.C. (1999). Forelimb kinematics and joint moments during the swing phase of the trot. Equine Vet. J. Supplement 30, 235-239. Singleton, W.H., Clayton, H.M., Lanovaz, J.L. Prades, M. (2003) Effects of shoeing on forelimb swing phase kinetics of trotting horses. Vet Comp Orthop Traum (in press). Willemen, M.A. (1997) Horseshoeing, a biomechanical analysis. PhD Thesis. Utrecht University. Willemen, M. A., Savelberg, H. C. C. M., Bruin, G., & et al. (1994). The effect of toe weights on linear and temporal stride characteristics of Standardbred trotters. Vet Quart, 16, S97-S100. Willemen, M. A., Savelberg, H. C. C. M., Jacobs, M. W. H., & Barneveld, A. (1996). Biomechanical effects of rocker-toed shoes in sound horses. Vet Quart, 18, Suppl 2, S75-S78.