Limb Movement Pattern in Forelimb and Hindlimb Lameness

The fetlock and coffin joints represent the loading pattern of the limb.Increasing lameness is indicated by decreased midstance excursions of the fetlock and coffin joint. Proximal joints adapt actively to lameness by increasing flexion during midstance in the lame limb. Carpal or tarsal joint lameness is characterized by reduced carpal/tarsal flexion during the swing phase. Carpal (swing) and fetlock (stance) joint pattern can be used for quantification of both the swinging and supporting of limb lameness.

1. Introduction

The kinematic analysis of the gait of lame horses started by the end of the 19th century with the beginning of kinematography [1]. In his famous book Animals in Motion, Eadweard Muybridge [1] not only presented a fascinating series of animal and human movements, but also various gaits and performances of horses, including those of three lame horses suffering from forelimb or hindlimb lameness. The sequences of photo plates show typical lameness symptoms as the asymmetric head movement pattern. Lameness, generally defined as an alteration of the normal gait caused by a functional or structural disorder in the locomotor system, is a synthesis of the movements of all parts of the body with each body segment adjusting its specific movement pattern to the lameness cause [2,3]. The trunk represents the major part (≈65%) of the total body mass, and its vertical load is responsible for the main part of the forces acting on the limbs [4]. Trunk movement is usually observed as movement of the withers, the back, the tuber sacrale, or the tuber coxae. The head and the neck add another 10% of mass, and typical head movements, acting with a long moment arm on the trunk, are used by lame horses to influence limb loading and by veterinarians as useful lameness indicators. The limbs have to carry the total body mass and perform forward movement. If loading (supporting limb lameness) or moving (swinging limb lameness) of the limbs causes pain, horses change limb timing, stride pattern, and limb joint movement pattern in all limbs to cope with the pain.

This paper describes the kinematic pattern of limb movement in lame horses. It explains general mechanisms of lameness compensation that can be found in proximal and distal limb joints. General principles, specific patterns in forelimb and hindlimb lameness, and supporting and swinging limb lameness are discussed.

2. Materials and Methods

Horses

Studies of the locomotion of lame horses use two different approaches to detect the characteristic changes caused by lameness. The first approach is the recording of patients, being either exemplary recordings of single horses with various different lameness causes [5-9] or cohorts of horses with the same defined lameness diagnosis [10-13]. The second approach tries to eliminate the problem of individuality in the locomotion pattern by using lameness models of sound horses; thus, the locomotion patterns of the sound horses are used as individual controls. Such kinematic studies are available for lameness caused by pain in the hoof [14-17], the superficial digital flexor tendon [18], and the carpal and tarsal joints [19-22].

Kinematic Methods

Recording Equipment

Several different technical systems have been used to record kinematic data of equine locomotion [23]. Starting with kinematography [5,11,24], efficacy of recording and data analysis improved with the introduction of optoelectronic and videographic methods. Depending on the number of cameras, two-dimensional or three-dimensional coordinates of selected anatomical landmarks on the skin of horses can be recorded.

Kinematic Markers

The recording of body movements is based on the selection of specific landmarks of the body. For limb kinematics, prominent bony landmarks (the tuber spinae scapulae) or the estimated centres of rotation of limb joints (the fetlock joint) are typically marked. Such "markers" are either active markers, sending light signals to a camera [a], or passive markers, reflecting light from special light sources [b,c] or detecting light flashes [d]. A typical marker set for limb movement recordings is based on the definitions of joint angles by Schmaltz [25] and uses the following marker locations at the forelimbs: the dorsal and the lateral hoof wall, the proximal insertion of the lateral collateral ligament of the metacarpophalangeal joint, the head of the lateral splint bone, the processus styloideus lateralis of the radius, the proximal insertion of the lateral collateral ligament of the elbow joint, the caudal part of the tuberculum majus, the tuber spinae scapulae, and the withers. Hindlimb markers are usually located at the dorsal and the lateral hoof wall, at the proximal insertion of the lateral collateral ligament of the metatarsophalangeal joint, at the head of the lateral splint bone, at the lateral malleolus of the tibia, at the proximal insertion of the lateral collateral ligament of the stifle joint, at the trochanter major of the femur, and at the ventral part of the tuber coxae.

These skin markers are prone to skin displacement errors, especially at the proximal joints [26] and the pastern region [27]. Studies on skin displacement compared fixed bone markers to skin markers and allowed for correction of kinematic data where necessary [28,29]. Most studies, however, do not use absolute joint angle values; instead, they use standardized joint angles (e.g., to the standing position [19]) or compare the angles of the same horse under different conditions, where the influence of skin marker artefact can be neglected. Advanced recordings of the three-dimensional movement of the limb segments need more sophisticated marker placement with at least three markers on each limb segment [30-32].

Data Analysis and Kinematic Variables

The data analysis of the marker coordinates follows similar procedures regardless of the recording equipment [23]. The typical steps of the data analysis start with the calibration of the recording system and the digitalization of the coordinates of the body markers. Digitalization may be done manually, semiautomatically, or fully automatically, depending on the software and recording environment (controlled light) available. The transformation process uses the digitized coordinates together with the calibration information to scale the data into three-dimensional coordinates. Smoothing is necessary to eliminate errors caused by digitalization. Normalization or standardization of the data allows for simple comparisons between different horses. The processed three-dimensional coordinates of the markers can then be used for the quantification of the marker movement itself, such as vertical or forward/backward movement, velocity, or acceleration. The marker coordinates can also be used to calculate joint angles of the various limb joints. These joint angles are typically presented as movements in a two-dimensional plane, such as sagittal flexion/extension, transversal adduction/abduction, or internal/external rotation. The joint movement nomenclature usually follows anatomical definitions of muscle function and describes flexion as having positive joint angle values and negative extension values.

After the calculation of all kinematic variables, the results are processed using general statistical procedures, which includes averaging repeated strides during one recording session and comparing different conditions in a group of horses or between horse groups.

3. Results

Distal Limb Lameness

Distal limb lameness is typically described as a supporting limb lameness, which means that pain primarily originates from the loading of the limb during the stance phase and that movement during the swing phase is less painful. Kinematic data are available for hoof lameness induced by the sole pressure model [15-17] as well as for patients suffering from navicular disease [11,13]. In the analysis of the locomotion pattern of horses suffering from distal limb pain, two different patterns can be seen in the proximal (shoulder, tarsal/stifle joint) and the distal limb joints (metacarpophalangeal, metatarsophalangeal [fetlock] and distal interphalangeal joint [coffin joint]). These patterns are similar for walk and trot, but higher vertical forces at the trot make the changes in this gait more easily observed.

Fetlock Joint

In sound horses at the trot, the fetlock joint shows the typical kinematic pattern (Fig. 1): after the landing of the hoof, the fetlock joint extends to maximal loading at midstance. Then, the joint starts flexing and reaches a similar joint angle at lift off as at landing [33]. During the swing phase, some passive flexion and extension occurs in preparation for extension before the next impact. This active extension by the digital extensor muscles is necessary for controlled landing on the limbs. The amount of hyperextension during stance is strongly correlated to vertical limb loading, which is quantified as vertical ground reaction force on a force plate [34,35]. This is caused by the passive, elastic nature of the suspensory apparatus of the fetlock joint, including the suspensory ligament and the proximal and distal check ligaments of the superficial and deep digital flexor tendons. Furthermore, superficial and deep digital flexor muscles act mainly as modulators of tendon strain and change the length of the muscle tendon unit very little [35]. We can use the fetlock joint as a natural and reliable force indicator; the only restriction is our optical capacity to detect small joint angle differences. Therefore, the amount of limb loading, both in the sound and lame horse, can be quantified kinematically by measuring the maximal fetlock hyperextension. With increasing lameness, fetlock hyperextension during midstance decreases (Fig. 1A). This decrease is ≈8° for a 2/5° forelimb lameness [3]. In the sound contralateral forelimb, a compensatory increase in hyperextension can be seen; however, the change is smaller (≈2°) than the reduction in the lame limb (Fig. 1B). Additional compensatory mechanisms keep the increase of load in the contralateral limb minimal. The fetlock joint angle as an indicator of limb loading can also be used to check hindlimb loading in forelimb lameness and to evaluate the limb load redistribution from the lame limb to other limbs (Fig. 2). On one hand, the diagonal hindlimb shows no change during forelimb lameness; the vertical load of this limb remains unchanged. On the other hand, the ipsilateral hindlimb, which loads simultaneously with the sound forelimb, is slightly unloaded. This indicates a hypercompensation of the lameness by the contralateral forelimb. In hindlimb lameness, the same analysis reveals the same compensation mechanism from lame to sound hindlimb, but no significant amount of weight is redistributed to the forelimbs (Fig. 3). These results correspond to a complete kinetic analysis of force redistribution in forelimb and hindlimb lameness as published by Weishaupt et al. [36,37].

Figure 1. Fetlock joint angle pattern of the lame (A) and contralateral sound (B) forelimb of one horse with 2° of induced forelimb lameness at the trot. Green line, sound condition; blue line, slight lameness; red line, moderate lameness.  

Figure 2. Mean maximal fetlock hyperextension of 11 horses with 2° of induced forelimb lameness at the trot.  

Figure 3. Mean maximal fetlock hyperextension of 11 horses with 2° of induced hindlimb lameness at the trot.  

Coffin Joint Movement

The coffin joint shows a flexion after the landing of the hoof and during the first 15% of the stride. Maximal flexion occurs before midstance, earlier than fetlock maximal hyperextension; then, the coffin joint extends till the moment of heel off [16]. A rapid flexion of the coffin joint corresponds to the rotation of the hoof around the toe between heel and toe off. During the swing phase, little movement occurs. In a lame limb, the coffin joint movement is changed similarly to the fetlock joint movement pattern. With increasing lameness, maximal coffin joint flexion during the stance phase in the lame limb is reduced, whereas maximal joint flexion in the contralateral limb is increased.

The carpal joint stays in a locked extended position during the stance phase and does not change during slight or moderate distal limb lameness. In this position, the carpus transfers the load from trunk and proximal limb to the distal limb joints. At the end of the stance phase, carpal joint flexion starts earlier in the lame limb than in the sound limb [10].

The fetlock/coffin joint complex acts as a passive spring in the equine limb construction. Additionally, the proximal limb joints (shoulder/elbow or tarsus/stifle and hip) act as a second spring in the total limb system [35]. However, they do not show a pure passive pattern, and their flexion and extension is modulated to react to the pain in the distal limb. Differing from the fetlock joint, there is no reduced flexion during midstance caused by reduced limb loading. Instead, there is an increase in flexion [16]. Although this increase is only small in the shoulder joint during forelimb lameness, tarsal/stifle joint flexion shows a more distinct increase in joint flexion during maximal loading. This can be interpreted as a softening of the proximal limb spring and an active reduction of the peak forces acting on the distal limb.

The excursions of the whole limb during one stride can be described as protraction and retraction of the limbs. During lameness, a characteristic, surprising change in this pattern can be observed. While protraction and retraction of the lame limb hardly changes, protraction in the contralateral sound limb increases and its retraction decreases (Table 1) [13,16,18]. Additionally, the step length, the distance between the hooves of two contralateral placements, is clearly reduced from lame to sound limb, but not from sound to lame limb. The explanation for this seemingly contradictory phenomenon lies in the significant reduction or absence of the suspension phase after the lame stance [15]. This stance phase of the lame limb is not shorter than stance duration in the same limb without lameness. During this painful stance phase, the sound limb is earlier and further protracted, compensating for the missing flight phase (suspension phase) after the lame stance [16]. This pattern was similar in distal forelimb and hindlimb lameness of the hoof [16], in horses suffering from navicular disease [13], and in a tendonitis study [18].

Summarizing the kinematic pattern of distal limb lameness, the uniformity of the changes in limb movements in the various lameness studies is impressing. Distal limb movement represents the reduced loading of the lame limb as a passive indicator system. Proximal limb movement shows an active reaction and smooths the loading of the painful limb. However, the described limb lameness compensation pattern causes a significant reduction of the body load. This load reduction is possible only by the altered vertical movements of the trunk, head, and neck.

Carpal and Tarsal Lameness

Few kinematic studies describe the typical pattern of lameness caused by ailments of the proximal parts of the limbs. Usually, proximal lameness causes pain not only during the loading of the limb (the supporting limb lameness component) but also during the swing phase. The protraction of the limb with flexion of the limb joints is painful. A typical example for such a mixed lameness is a carpal or tarsal lameness. Ratzlaff et al. [10] analyzed a series of horses with naturally occurring carpal lameness using goniometry (measuring of the joint angle with a goniometer). Induced carpal lameness was evaluated kinematically by Back et al. [19] and Peloso et al. [20]. The main finding in these studies was a reduced flexion of the carpal joint during the swing phase. Flexion of the carpal joint causes pain and is reduced in correlation to the lameness degree. Therefore, Back et al. [19] suggested the use of this maximal carpal flexion as a kinematic indicator for the swinging limb lameness component together with the maximal fetlock hyperextension as an indicator of the supporting limb lameness component.

Similar results were reported for induced tarsal synovitis of the distal tarsal joints (tarsometatarsal and distal intertarsal) [22]. Even pain in these tight joints causes decreased flexion of the talocrural during both stance and swing phase as well as decreased fetlock joint hyperextension during stance. This indicates that they are both components of a mixed lameness.

4. Discussion

The kinematic pattern of limb movement reveals two different spring-like systems. The distal spring consists of the fetlock and the coffin joint and represents, by its passive nature, the loading pattern of the limb. The proximal spring consists of the shoulder/elbow joints or the tarsal/stifle and hip joint complex. The proximal spring can adapt actively to lameness by increasing flexion during midstance in the lame limb, which smooths out the loading of the painful limb. The distal joints indicate reduced loading in the lame limb by decreased midstance excursions (i.e., reduced hyperextension of the fetlock joint and reduced flexion of the coffin joint). Correspondingly, the fetlock joint of the contralateral limb shows some compensating increase of hyperextension but to a smaller amount than the decrease of the lame limb. Carpal or tarsal joint lameness is characterized by reduced carpal/tarsal flexion during the swing phase. Carpal (swing) and fetlock (stance) joint patterns can be used for quantification of both the swinging and supporting components of limb lameness.

Footnotes

[a] Selspot Motion Measurement System, Innovision Systems, Warren, MI 48093.
[b] Expert Vision, Motion Analysis Corp., Santa Rosa, CA 95403.
[c] ProReflex, Qualisys Inc., Glastonbury, CT 06033.
[d] CODA, Charnwood Dynamics Ltd., Leicestershire, LE7 7PJ, UK.