LAMENESS DYNAMICS
(Presented by Dr. Hilary Clayton at the Wild West Veterinary Conference, October, 1997)
 

Contents:

Introduction

Abbreviations

GRF: ground reaction force
DAL: distal accessory ligament
DDFT: deep digital flexor tendon
SDFT: superficial digital flexor tendon
SL: suspensory ligament

Most breakdowns result from the effects of limb loading during the stance phase of the stride. Occasionally, a single catastrophic event is identified as causing an injury. More often, it is the repeated limb trauma during training and competition that results in overuse or fatigue injuries, which precede a major breakdown. For example, in Thoroughbreds intensive exercise schedules in which horses accumulate large distances at racing speeds, have been implicated as a predisposing factor for fatal skeletal injury (Estberg et al., 1995).

Loading of the limbs during the stance phase occurs in 2 stages. During the impact phase, which occurs immediately after the hoof contacts the ground it is rapidly decelerated giving rise to an impact shock wave that travels proximally in the limb. This type of loading is particularly damaging to the bones and joints. During the remainder of the stance phase, the limb accepts the body weight then pushes off against the ground. It is during this stage that the soft tissues are particularly vulnerable. An understanding of the characteristics of the impact phase and the stance phase leads to a better appreciation of the causes of lameness in athletic horses and to the development of strategies for preventing and treating problems.
 

Limb Loading During Locomotion

Impact Phase

Repetitive limb loading during locomotion generates intermittent waves of deceleration that are attenuated by the body’s natural shock absorbers as they travel proximally in the limbs. The impact shock wave is characterized by accelerations of high amplitude with a rapid vibration frequency, that peak within 50 milliseconds after the foot contacts the ground. The duration of the impact phase is shorter than the neuromuscular response time, which precludes muscular intervention in response to events during the impact phase (Nigg et al., 1995). Some of the energy that enters the locomotor system when the foot strikes the ground is dissipated through attenuation by the body tissues. Consequently, the amplitude of the impact shock wave decreases as it travels proximally in the limb. Ineffective attenuation of impact shock, which causes microtrauma to bone and articular cartilage, has been shown to play a primary causative role in acute and chronic skeletal and articular injuries. In contrast to the high amplitude and high frequency loading in the impact phase, in the later part of the stance phase, limb loading occurs gradually and without high frequency oscillations. Since the behavior of the musculoskeletal tissues depends on the rate of deformation, the tissues react differently during impact than during the later part of the stance phase.

In horses, impact shock is likely to be an important etiological factor in acute breakdown injuries, e.g. long bone fractures, and in chronic traumatic problems, e.g. degenerative joint disease. Catastrophic fractures of the long bones during racing or training are often preceded by fatigue fractures (Stover et al., 1992), which have been identified as a consequence of impact loading (Radin et al., 1973). In short bones and sesamoid bones, sclerosis occurs prior to fracture in well-defined patterns that are related to the stress lines (Pool, 1992); sclerosis of subchondral bone is also a consequence of impact loading (Radin et al., 1973).

Even at relatively slow speeds of around 4 m/s the hoof experiences impact accelerations in the order of 80 to 100 g (Benoit et al., 1993). The amplitude and vibration frequency of the shock wave vary with gait, speed, fatigue, ground surface and shoeing. Both the amplitude and vibration frequency increase with speed. The onset of fatigue is associated with a significant increase in amplitude of the impact shock in human beings and in horses (Pratt et al., 1976). Therefore, muscular fatigue may play a role in impact related injuries. Steel shoes increase the amplitude, whereas certain shoes and pads reduce both the amplitude and frequency of the impact accelerations on the hoof wall (Benoit et al., 1993). The amplitude also increases with the density of the surface material, but is reduced when the surface has a higher content of water or organic material (Barrey et al., 1991). Measurement of the properties of the work surface with a mechanical testing device is not entirely representative of the biological behavior of the hoof of a moving horse; a hoof mounted accelerometer is a more valuable testing device.

The hoof acts as the initial shock absorber for the skeletal system by absorbing impact shock in the laminae and digital cushion. Our studies of cadaver limbs  (Lanovaz, 1997) indicate that the soft tissues inside the hoof, such as the laminae and digital cushion, are primarily responsible for attenuating the frequency of the impact vibrations, whereas the bones and joints are more important for attenuating the amplitude. As the shock wave travels up the limb, the subchondral bone, articular cartilage and other periarticular tissues aid in its absorption and dissipation. Subchondral bone is a fairly efficient shock absorber, but excessive impacts lead to sclerosis and microfractures. Articular cartilage is an even more effective shock absorber than an equivalent amount of bone, but because it is present in such a thin layer in the joints it makes a relatively small contribution to overall shock attenuation. There is evidence that articular cartilage is fatigue prone, and there may be a threshold of impulse intensity above which cartilage damage is progressive and irreparable. Changes in cartilage in response to impact loading include metabolic and biochemical alterations that are consistent with cartilage degeneration and the development of osteoarthritis. Degenerative joint disease further reduces the ability of the joint to attenuate impact shock, resulting in damage to the more proximal and distal joints. The role of exercise in initiating and perpetuating damage to articular cartilage in degenerative joint disease is well-established. For example, sheep housed on concrete floors are more prone to develop osteoarthritis than those housed on dirt due to the effects of repeated impulsive loading over a prolonged period.

Stance Phase

The carpus rapidly snaps into the close-packed position after initial ground contact, which allows the fore limb to act as a propulsive strut throughout most of the stance phase. The fetlock joint and the palmar soft tissues behave like an elastic spring to conserve energy. In the early part of the stance phase the fetlock joint dorsiflexes as it sinks toward the ground, reaching its lowest point at midstance, which corresponds with the time when the cannon bone is vertical. As the fetlock joint dorsiflexes, the palmar soft tissues are stretched. After midstance the fetlock rises allowing the elastic structures to recoil, thereby releasing the elastic energy that was stored during the stretching process. Flexion of the coffin joint in the early stance phase assists the fetlock joint in absorbing concussion but the coffin joint reverses its direction of motion before midstance and continues to extend until the terminal part of breakover.

During the stance phase, the functions of the limbs are to accept the body weight in the early part of stance then to push off against the ground in the later part of stance. The forces between the hoof and the ground are measured in 3-dimensions: vertical, longitudinal (from head to tail) and transverse (mediolateral). The transverse forces are small in magnitude and show much variation between horses and even within an individual horse. Because of this variability, the transverse forces have not been studied in detail. Much more attention has been paid to the vertical and longitudinal forces (figure 1). The vertical force is always positive; it is responsible for overcoming the effects of gravity and for raising the body mass. At the trot, the vertical component of the GRF peaks at midstance, when the cannon segment is vertical and the fetlock is at its lowest position. The longitudinal force is concerned with retardation (deceleration) and propulsion (acceleration) of the horse in a forward direction. The longitudinal force normally shows negative and positive components during each stance phase as the horse's body rolls forward over the limb. In the early part of the stance phase, the longitudinal force retards the forward movement, later in the stance phase it provides propulsion. The direction of the longitudinal force changes around the time of midstance.

 
Figure 1: Vertical and craniocaudal forces on the forelimb of a trotting horse during the stance phase.
 

It is during the loading phase, which occupies the period from the end of the impact phase until midstance that the elastic structures on the palmar side of the limb are strained. These structures store elastic energy as they lengthen. In the unloading phase that follows midstance, the fetlock joint rises and the elastic structures recoil. The release of elastic energy helps to raise the horse's body into the suspension.

The DDFT, SDFT and SL are maximally strained at midstance, whereas the DAL is maximally strained at the start of breakover (figure 2). The entirely passive structures (SL, DAL) are loaded and strained more than the DDFT and SDFT which have an active muscular component that adjusts tension in the tendons. Maximal strains in the SDFT and DDFT are higher when the horse carries weight, moves on a hard surface or travels at higher speeds.

 
Figure 2:  Fore limb tendon strains during the stance phase at the trot.

The SL together with the sesamoid bones and the sesamaoidean ligaments acts as a passive system to support the fetlock. Since it has no muscular component, SL strain depends entirely on the angle of the fetlock joint. As the fetlock dorsiflexes, SL strain increases and reaches its maximal value at midstance. The extensor branches of the SL are taut in the period around ground contact. Their function is to orient the hoof for contact and to prevent buckling forward of the interphalangeal joints during the early stance phase.

The DAL also has no muscular component, and its strain depends on the angle of both the fetlock and coffin joints, though the coffin joint is considerably more influential. Maximal strain corresponds with the start of breakover. Due to its dependence on coffin joint angulation, the DAL is particularly sensitive to changes in hoof angle and toe length, and to different surface types in terms of the ability of the hoof to rotate during the stance phase.
 

Effects of Lameness

Lamenesses have traditionally been classified as supporting limb, swinging limb or mixed. Gait analysis shows that almost all lamenesses show deficits in both the stance and swing phases though one or other is likely to predominate. Changes in the stride timing vary with the limb and site of lameness. An absence of a suspension phase following the lame diagonal stance phase is a fairly consistent alteration.

In a predominantly supporting limb lameness, the horse carries less weight on the lame limb with corresponding reductions in the peak vertical force borne by the limb. This is reflected by reductions in coffin joint extension and fetlock joint dorsiflexion at midstance. There are compensatory increases in the contralateral (sound) limb. The maximal angles of the fetlock and coffin joints are one of the most consistent and sensitive indicators of lameness.

In contrast to the distal joints which show reduced flexion in the lame limb, the proximal joints, notably the shoulder in the fore limb and the tarsus in the hind limb, may show increased flexion in the lame limb. This is a load-damping effect that reduces the peak forces in the lame limb (Buchner et al., 1996).

The range of protraction and retraction of the limb as a whole may change when the horse is lame. With a fore limb lameness retraction of both fore limbs tends to be reduced, whereas with a hind limb lameness protraction of both hind limb tends to be reduced. This is because the fore limb is closer to the horse’s center of gravity (and carries more weight) when it is retracted, whereas the hind limb is closer to the center of gravity (and carries more weight) when it is protracted (Buchner et al., 1996). With regard to protraction and retraction, it is interesting to note that the hind limbs are retracted further during walking than during trotting. This explains why the signs of fibrotic myopathy, which affects the hind limb in the fully retracted position, are more obvious in the walk than in the trot.

The head, withers and tuber sacrale normally show a sinusoidal pattern in their vertical displacement during trotting. Changes in the head movement pattern are the best indicators of a fore limb lameness, with the head being raised during the lame fore limb stance phase and sinking during the sound fore limb stance phase. It has traditionally been assumed that the mechanism of action was through a static effect of shifting the center of mass caudally, but more recent studies suggest that this has only a minor effect and that the asymmetrical head movements have a greater effect through the inertial interaction between the trunk and the head/neck segment. The resultant reduction in neck joint sagittal torque reduces the maximal vertical force on the trunk (Vorstenbosch et al., 1995). During both fore and hind limb lamenesses at the trot, the trunk had a lower vertical velocity at impact of the lame limb, and during the lame limb stance phase the trunk was kept higher above the ground (Buchner et al., 1996). In effect, the sound diagonal pushes off into a suspension and, as a result, the trunk is highest at the start of the lame diagonal stance phase. It sinks gradually during the lame diagonal stance phase, and as weight is transferred from the lame to the sound diagonal without the intervention of a suspension. After midstance on the sound diagonal the trunk is again raised into a suspension in preparation for the next stance phase of the lame diagonal.

The best indicator of a hind limb lameness is the movements of the hips and croup. When a trotting horse is viewed from behind, the oscillations of each tuber sacrale are asymmetrical even in the sound condition, such that there is a greater elevation during the stance phase of the contralateral limb, in other words when the limb is being protracted during its swing phase. During hind limb lameness, movement of the tuber coxae is increased on the side of the lame limb (Buchner et al., 1996). The asymmetry is perceived most easily just before ground contact of the lame limb when the tuber coxae on that side is elevated rapidly. These movements can also be seen by watching the croup movements in the lateral view; the croup is highest just before the lame limb makes contact with the ground.
 

References

Barrey, E., Landjerit, B., & Wolter, R. (1991). Shock and vibration during the hoof impact on different track surfaces. S. G. B. Persson, A. Lindholm, & L. B. Jeffcott, (Eds.), Equine Exerc Physiol (pp. 97-106). Davis, California: ICEEP Publications.

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.

Buchner, H. H. F., Savelberg, H. H. C. M., Schamhardt, H. C., & Barneveld, A. (1996). Head and trunk movement adaptations in horses with experimentally induced fore- or hindlimb lameness. Equine Vet J, 28(1), 71-76.

Buchner, H. H. F., Savelberg, H. H. C. M., Schamhardt, H. C., & Barneveld, A. (1996). Limb movement adaptation in horses with experimentally induced fore- or hindlimb lameness. Equine Vet J, 28(1), 63-70.

Estberg, L., Stover, S. M., Gardner, I. A., Drake, C. M., Johnson, B., & et al. (1995). Several racing-career intersity characteristics are associated with racing-related fatal skeletal injury in California Thoroughbred horses. Proc Am Assoc Equine Practnr, 41, 82-83.

Lanovaz, J. (1997). In vitro impact attenuation characteristics of equine digits. Masters Thesis, University of Saskatchewan, Saskatoon, Saskatchewan.

Nigg, B. M., Cole, G. K., & Bruggemann, G.-P. (1995). Impact forces during heel toe running. J Appl Biomech, 11, 407-432.

Pool, R. R. (1992). Third carpal bone injuries. Equine Vet Data, 16, 279.

Pratt, G. W., & O'Connor, J. T. Jr. (1976). Force plate studies of equine biomechanics. Am J Vet Res, 37, 1251-1255.

Radin, E. L., Parker, H. G., Pugh, J. W., & et al. (1973). Response of joints to impact loading - III Relationship between trabecular microfractures and cartilage dgeneration. J Biomech, 6, 51-57.

Stover, S. M., Johnson, B. J., Daft, B. M., & et al. (1992). An association between complete and incomplete stress fractures of the humerus in racehorses. Equine Vet J, 24( ), 260-263.

Vorstenbosch, M. A. T. M., Buchner, H. H. F., Savelberg, H. H. C. M., Schamhardt, H. C., & Barneveld, A. (1995). Compensatory head movments in the lame horse: a model study. H. H. F. Buchner Lameness management in horses: a kinematic study (pp. 87-98). Utrecht, The Netherlands: PhD Thesis.