The effect of gait and digital flexor muscle activation on limb compliance in the forelimb of the horse Equus caballus
Structure and Motion Laboratory, Veterinary Basic Sciences, The Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire AL9 7TA, UK
* Author for correspondence at present address: School of Biology, L. C. Miall Building, University of Leeds, Leeds LS2 9JT, UK (e-mail: m.p.mcguigan{at}leeds.ac.uk)
Accepted 19 January 2003
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Summary |
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Key words: locomotion, gait, stiffness, tendon, horse, Equus caballus
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Introduction |
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There is, however, a disadvantage in having a forelimb with mainly passive
properties. Humans can change limb compliance as a function of surface
compliance and stride frequency (Farley
and Gonzales, 1996; Farley et
al., 1998
; Ferris and Farley,
1997
). In this situation the muscles either store energy in the
tendon, for subsequent release in a catapult mechanism when the muscle-tendon
unit/limb is unloaded, lengthen and shorten to emulate spring-like properties,
or preload the tendon and hence stiffen the spring (due to the non-linear
force-length properties of tendon). As the muscle fibres become short in
proportion to the tendon length there is less scope for control in the system,
since the limited shortening of the associated muscle will only stretch the
tendon rather than causing movement at the insertion
(Biewener and Roberts,
2000
).
In the horse the ground reaction force acts approximately along the axis of the leg from the foot to close to the attachment of serratus ventralis (J. Watson and A. M. Wilson, unpublished data). The leg changes length along this axis by flexion of the limb joints and can be considered as two compression springs in series.
The distal spring
The distal spring is the limb below the elbow joint, with length change
occurring by extension of the metacarpo-phalangeal (MCP) and distal
interphalangeal (DIP) joints.
Extension of the metacarpo-phalangeal joint during stance is resisted by
three specialised muscle tendon units: the superficial and deep digital
flexors (SDF, DDF) and the suspensory ligament (SL)
(Dyce et al., 1987)
(Fig. 1). These three
structures are loaded to high strains and forces during locomotion
(Biewener 1998a
;
Dimery et al., 1986
;
Meershoek et al., 2001
;
Stephens et al., 1989
) and
approx. 50% of racehorse injuries occur in these tendons
(Williams et al., 2001
). The
SL, an evolutionary modification of the interosseus muscle, is completely
fibrous, with in young animals, at most, only remnants of muscle fibres. The
superficial digital flexor muscle is almost completely fibrous in the hind
limb and in the forelimb has fibres of length 2-6 mm
(Biewener, 1998b
;
Dimery et al., 1986
;
Hermanson and Cobb, 1992
). The
deep digital flexor muscle has three heads, humeral, radial and ulnar. The
largest of these, the humeral head, has a mass of approximately 400 g and can
be divided into three compartments by fibre length. The fibres are 7±1
mm in the short-fibre compartment, 18±1 mm in the intermediate-fibre
compartment and 112±13 mm in the long-fibre compartment (M. P. McGuigan
and R. Hagan, unpublished data). The radial and ulnar heads are much smaller
with fibres of approximately 17 mm
(Hermanson and Cobb, 1992
).
The SDF and DDF muscles are force-protected by accessory ligaments
(Dyce et al., 1987
) that link
the tendon distal to the muscle belly to the bone
(Fig. 1). The force generation
capacity of these muscles is about 5 kN (predicted from calculations of
physiological cross-sectional area). The deep digital flexor muscle was shown
to exert a force of about 3 kN in horses with chronic foot lameness
(Wilson et al., 2001a
). In
those studies the effect of DDF muscle contraction was to stretch the
associated tendon, since no change in foot position was observed. In a
previous study we have, however, shown that, in vitro, the digital
flexor muscles are only capable of a length change of a few millimetres
(Wilson et al., 2001b
).
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The proximal spring
The proximal spring represents the limb between the scapula and the elbow,
with length change along the ground reaction force (GRF) vector occurring
via linked flexion of the shoulder and the elbow
(Fig. 1).
Elbow flexion is resisted by the large triceps muscle and by the digital
flexors (which have an extensor moment at the elbow), and shoulder flexion by
the biceps and supra spinatus muscles and a number of other muscles
(Dyce et al., 1987)
(Fig. 1). The other muscles of
the shoulder either have small moment arms on the joint and appear to act as
stabilisers preventing out of sagittal plane movements, or are long-fibred and
likely to be involved in limb movement rather than resisting gravitational and
inertial forces.
The proximal limb spring is therefore both muscular and collagenous in nature (Fig. 1). The relative role of the two leg springs is of interest. One possible role is that the proximal spring acts in series with the mainly passive distal limb spring to tune the properties of the whole limb for locomotion under varying conditions. This mechanism could be simply via the mechanical effect of two springs in series and changing the stiffness of the proximal spring via muscle contraction. In addition, changing the elbow angle by muscle contraction will change the zero length of the digital flexor muscles. Due to alterations in load distribution between the long and compliant muscle belly and the short and stiff accessory ligament, this would also have a tuning effect on leg stiffness. Alternatively, the proximal spring muscles may act to drive the distal spring, either by a power flow across the elbow or by shortening in late stance as the leg unloads.
Muscle shortening during stance is, however, energetically expensive, due
to the high forces in the muscles that resist the ground reaction force and
the relatively long muscle fibres that are required. Optimisation of the
musculoskeletal system for economical locomotion would therefore suggest that
length change should occur in the distal, passive, spring and that the muscles
of the proximal spring would remain isometric during stance. Length change in
the proximal spring would therefore be limited to elastic deformation of the
elastic elements of the muscle tendon unit. Biceps, in addition to its
antigravity role, functions as the spring in a catapult mechanism to protract
the limb (Wilson et al.,
2003).
The attachment to the trunk could be considered as a third spring, which is muscular in nature, but that will not be discussed further here.
The present work reports the results of a series of experiments where the compliance of the limb under varying locomotor conditions was examined, with the aim of determining if a horse can alter limb compliance.
This study tested the following two hypotheses: (1) the majority of the length change in the equine forelimb occurs below the elbow joint in the collagenous distal limb; and (2) the relationship between MCP joint angle and limb force is similar for limbs loaded in vitro and in vivo, and is not altered by contraction of the digital flexor muscles in vitro or by changing gait in vivo.
Four experiments were undertaken. (1) Length changes in the proximal and distal forelimb during stance phase of locomotion were measured at a range of speeds and gaits on the treadmill. (2) The MCP joint anglelimb force relationship in vitro, and how it is altered by contraction of the digital flexor muscles, and (3) in vivo, and how it is altered by gait, were examined. (4) The peak vertical GRF at gallop was estimated from the MCP joint anglelimb force relationship.
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Materials and methods |
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The horses were then exercised on a high-speed treadmill. The positions of the markers were recorded using a 3-D video motion analysis [ProReflex 2.5, Qualisys AB, Göteborgsvägen 74, SE-433 63, Sävedalen, Sweden (www.Qualisys.com)] system positioned approximately 2 m to the left of the treadmill.
The horses were fully habituated to the treadmill (Sato, Upsalla, Sweden)
(Buchner et al., 1994) and
were exercised on it regularly. During the test they wore neoprene brushing
boots and over-reach boots to avoid interference injuries while galloping at
high speed.
After a warm up period of 5 min walk and 5 min trot, data were recorded at 120 Hz during the last 10 s of a 1 min period of trot (3.5 m s-1), canter (6 m s-1 and 8 m s-1) and gallop (12 m s-1).
The cranio-caudal and vertical position of the markers on the proximal spine of the scapula, the centre of rotation of the elbow joint and the hoof wall were determined at the beginning of the stance phase and at mid-stance. The beginning of the stance phase was taken to be the time point at which the vertical coordinate of the foot marker became constant at the end of the protraction phase, and mid-stance was defined as the time point at which the metacarpal bone was vertical (i.e. the marker at the proximal end of metacarpal IV was above the marker at the MCP joint). From these coordinates the lengths of the proximal and distal portions of the limb were calculated using Pythagarus' theorem in a spreadsheet program (Excel 97, Microsoft, USA).
The proximal spring length was defined as the distance between the proximal spine of the scapula and the elbow joint, and the distal spring length as the distance between the elbow joint and the hoof. The length change during stance was defined as the difference between the values at the beginning of stance and mid-stance. These were expressed as absolute length changes and ratios of proximal:distal length changes.
(2) In vitro MCP joint anglelimb force relationship
Tissue was collected from horses of varying size, breed and age, euthanased
at the Royal Veterinary College and an equine abattoir for reasons other than
orthopaedic problems. Immediately post mortem one forelimb was
removed and prepared for loading in a hydraulic testing machine.
Mounting the limb
Limbs were sectioned with the humeroradial (elbow) joint held at an
angle similar to that seen at mid-stance (230-235°). The limbs were cut
with a saw at right angles to the long axis of the distal limb just proximal
to the humeral epicondyles, leaving the olecranon intact. A 13 mm diameter
hole was drilled vertically down from the marrow cavity of the distal humerus
through the elbow joint articulation and into the radius. The limbs were
mounted in the hydraulic loading jig (Clarke machinery 020410000,
www.machinemart.co.uk)
by means of a 130 mm pin, which was positioned vertically down through the
elbow joint and attached to a hydraulic ram. The pin was placed down the
drilled hole so that the sectioned humerus rested on the face of the ram. The
ram face provided a 50 mm diameter flat loading surface. This pin locked the
elbow joint to prevent any change in joint angle during loading but was not
rigidly fixed to the ram, to allow craniocaudal movement of the
intermediate segments of the limb (Wilson
et al., 2001b). The hoof of the limb was positioned on a base
plate. Compression of the ram resulted in compression of the limb and
extension of the carpus, MCP and DIP joints.
In order to stimulate the digital flexor muscles and assess the effect of stimulation, the limbs were prepared as follows: flexor carpi radialis, flexor carpi ulnaris and extensor carpi ulnaris were removed. The tendons on the dorsal aspect of the limb of the digital extensor muscles and extensor carpi radialis were sectioned proximal to the carpus (this was done to prevent voltage leakage from the stimulator causing activation and force generation of these muscles).
The digital flexor muscles were stimulated using an electrical stimulator under the control of a signal generator, and clean 128-strand copper wires placed proximally and distally in the muscles. The stimulator supplied a 60 V signal at 50 Hz with a pulse duration of 0.06 ms. Once the electrodes were in place the muscles were wrapped in plastic film to prevent evaporative cooling. The experiments were completed by 1 h post mortem.
Measurements
The hoof of the limb was positioned on a foot-plate. A shear beam force
transducer (Transducer World, Aylesbury, Buckinghamshire) placed under the
foot-plate recorded axial limb force, logged at 100 Hz via software
written in LabView [National Instruments, Newbury, Berkshire RG14 5SJ, UK
(www.natinst.com)].
The amplified output from the force transducer was displayed on a voltmeter so
that limb force could be controlled during the loading cycles. The output from
the signal generator was also logged via LabView.
MCP joint angle and limb length were calculated from kinematic data collected at 100 Hz using a 2-D video motion analysis system (ProReflex 2.5). Flat, circular retro-reflective markers 10 mm in diameter were placed at the following anatomical landmarks to facilitate calculation of MCP joint angle and the length of the limb during the compressive loading: the origin of the digital flexor muscles, the proximal end of metacarpal II, the proximal attachment of the lateral collateral ligament of the MCP joint to the distal metacarpal III and the lateral hoof wall approximately over the centre of rotation of the DIP joint.
Two flat markers were placed on the frame of the loading jig, 300 mm apart, for length-calibration purposes.
Simultaneous limb force, electrical stimulation and kinematic data were recorded for a period of 15 s while the limb was ramp loaded to approximately 1.25x body mass, with and without muscle stimulation. Four unstimulated and two stimulated (both DDF and SDF muscles) loading cycles were recorded. Recordings were made from six limbs in the unstimulated and stimulated states and a further three limbs in the unstimulated state only.
MCP joint angle (around palmar aspect) and limb length were calculated using trigonometry in a spreadsheet program and plotted against limb force for the loading phase of the cycle. Linear regression lines were calculated for each trial of each limb. A mean plot for unstimulated loading of each limb was generated and compared to the first and second stimulated loadings. Paired t-tests were used to compare the force required to produce an MCP joint angle of 220° during the unstimulated loadings with the force required to produce the same joint angle during the first and second stimulated loadings.
(3) In vivo MCP joint anglelimb force relationship
Horses and riders
Seven thoroughbred-cross riding horses of mixed size and age were used.
They were all assessed as having a `normal' gait and being free from any signs
of lameness on veterinary examination. All the horses were accustomed to being
ridden in the indoor arena where the data were recorded. The data were
recorded during ridden locomotion and all the horses were ridden by riders
with whom they were familiar. Three different riders were used. The mass of
the horses was 548-667 kg and that of the riders 60-70 kg.
Experimental setup
A forceplate (Kistler 9827BA, Kistler Instruments Ltd. Alresford House,
Mill Lane, Alton, Hampshire GU34 2QJ) was buried half way along the long side
of an indoor riding arena (60 mx20 m). The mounting frame for the
forceplate was set in 1 m3 of concrete and the top of the plate was
level with the sub-base of the riding surface. The forceplate was topped with
an aluminium plate covered in a coarse surface conveyer belt matting and the
riding surface, 200 mm of sand and polyvinyl chloride (PVC), was laid on top.
The forceplate signal was amplified by integral eight-channel charge
amplifiers, filtered through a low-pass filter (6 db/octave from 50 Hz) and
logged via a 12-bit AD converter at 480 samples s-1 into a
personal computer using software written in LabView (National
Instruments).
The motion analysis system used above was placed to the left-hand side of the forceplate and calibrated relative to the forceplate to determine the position of the left forefoot relative to the plate and the left forelimb MCP joint angle during stance. Kinematic data were recorded at 240 Hz. The accuracy of the 3-D motion analysis system within a calibrated volume of 3 mx1 mx2 m was determined using a pre-calibrated grid and found to be within ±2 mm for absolute position measurements and less than ±0.1 mm for relative (i.e. length) measurements. Data logging for both systems was triggered using a light gate.
Recording protocol
Synchronised kinetic and kinematic data were recorded as each horse was
ridden over the forceplate at walk, trot and canter (leading with left and
right limbs), and jumped onto the forceplate until at least six left
forestrikes had been recorded. (The speed within each gait was that chosen by
the individual horses.) Data were rejected if the horse was not judged to be
moving freely and consistently in a straight line, or the foot was not
completely on the plate. The jump was a 750 mm high fence, situated 1.5-2 m in
front of the forceplate, which was jumped from a steady canter. The horses
were jumped onto the forceplate in an attempt to perturb the spring mass
system. Jumping perturbs the system as stance time and the angle of the limb
at impact are altered independently of speed.
Data analysis
Stance was defined as the period during which the vertical ground reaction
force was greater than 50 N (Clayton et
al., 1999). During analysis, data were rejected if the point of
application of the GRF on the forceplate was within 100 mm of the edge of the
plate. GRF data were normalised for the mass of the horse and rider and
interpolated to 100 points, evenly spaced throughout the stance period, to
allow the averaging of several strides
(Merkens et al., 1985
;
Wilson et al., 1998
). A plot
of vertical GRF (mean ± S.D.) was produced for each horse at each
gait.
MCP joint angle was defined as the angle around the palmar aspect of the limb and calculated from the craniocaudal and vertical positions of the three limb markers by simple trigonometry. Foot-on and foot-off were determined from the simultaneous forceplate data and the MCP joint angle data were was normalised for stance time; plots of MCP joint angle (mean ± S.D.) were produced for each horse at each gait.
The corresponding mean vertical GRF and MCP joint angle during stance were
plotted against one another to show the relationship between limb force and
MCP joint angle within the stance phase for each gait/horse combination. Two
linear regression lines were calculated for each of these plots: one for the
loading phase of stance (impact to peak vertical force) and one for the
unloading phase (peak vertical force to foot-off). The distribution of the
data used to calculate the regression lines was skewed towards the upper end
of the range due to the mid-stance plateau of the GRF curve
(Fig. 6), hence the regression
lines were weighted in that direction. The stiffness of the limb during the
loading and unloading phases of stance was taken as the gradient of the
respective regression line. This is not classical stiffness, since it is the
relationship between a linear force and an angle change; it is, however, a
useful measure for this study. The limb force associated with an MCP joint
angle of 230° was calculated from the regression line of the loading phase
of the MCP joint anglelimb force relationship for each horse at each
gait. These values were compared using a single-factor analysis of variance
(ANOVA) to determine if gait had a consistent effect on the relationship. In
all statistics, P0.05 was considered to be a significant
difference.
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Peak values of vertical GRF and MCP joint angle, and the time of the peak for each horse at each gait, were calculated. The peak vertical GRF and MCP values for each horse at each gait were plotted against each other to assess the relationship between the peak values across gaits and horses. A linear regression line was calculated for each set of data points and separately for all the points together. Whilst statistically suspect, this served to illustrate whether the relationship between peak vertical GRF and peak MCP joint angle varied between gait and horses.
(4) Estimation of peak vertical ground reaction force at gallop
Five fit thoroughbred horses Equus caballus, free from any sign of
lameness, were used in this part of the study (mass 524-678 kg).
Determination of limb forceMCP joint angle relationship at
trot
The forceplate was placed midway along a 25 m covered, concrete runway. The
runway and the forceplate were covered in 6 mm thick commercial conveyer belt
matting. The experimental setup was otherwise identical to that described
above in (3).
Retro-reflective markers were placed at the skeletal landmarks described above to determine MCP joint angle, and a fourth marker was placed on the thorax of the horse to determine speed during forceplate assessment. The horses were trotted, in hand, at a speed comfortable for the horse, along the runway until six left forelimb forceplate strikes had been recorded.
Data were analysed as described above and plots of vertical GRF and MCP joint angle (mean ± S.D.) during stance generated. Peak vertical GRF and MCP joint angles were calculated, and the linear regression line for the loading and unloading phase of the limb forceMCP joint angle relationship calculated.
MCP joint angle at gallop
The same five horses were exercised on the treadmill (a 8 mm thick conveyer
belt mat on a steel base plate with similar surface characteristics to the
overground runway) to determine the peak MCP joint angle at gallop. The horses
were habituated to the treadmill with three training sessions
(Buchner et al., 1994; T.
Richmond and A. W. Wilson, unpublished data). The experimental setup was
similar to that described in (1). The retro-reflective markers remained in
situ from the horses' overground assessment.
After a `warm up' period, kinematic data were recorded for 10 s at the end of a 60 s exercise period on the flat at gallop (12 m s-1). During the gallop test it was recorded whether the left forelimb was the lead or non-lead leg. We attempted to record trot data to verify that MCP joint angle was similar at the same speed of trot on the treadmill and overground, but unfortunately, a consistent trot could not be established on the treadmill at the over-ground speed. Maximum MCP joint angle during the stance phase was calculated for each stride and averaged for lead and non-lead limbs at gallop.
Peak vertical ground reaction force at gallop
The equations of the linear regression lines calculated for the limb
forceMCP joint angle relationship at trot overground were used to
predict the value of vertical GRF associated with the peak MCP joint angles
observed at gallop.
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Results |
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(2) In vitro MCP joint anglelimb force relationship
There was an excellent linear relationship (r2>0.99)
between the length of the limb and the force applied and MCP joint angle and
the force applied to the limb throughout the loading cycle for all the loading
trials (Fig. 2A,B).
Fig. 3 shows the linear
regression lines for the MCP joint anglelimb force relationship for the
nine limbs in the unstimulated state. The r2 values for
these lines were 0.989-0.996 and the mean slope of the line was
0.34±0.02 N kg-1 BM deg.-1, range 0.32-0.37 N
kg-1 BM deg.-1 in the different limbs. Six of the limbs
were loaded with stimulation of the digital flexor muscles. There was minimal
difference in the force required to produce a joint angle of 220° with
(6.50±0.48 N kg-1 BM) and without (6.45±0.41 N
kg-1 BM) contraction of the digital flexor muscles (values
calculated from the regression lines) (Fig.
4).
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(3) In vivo MCP joint anglelimb force relationship
Foot contact on the forceplate was difficult to confirm during data logging
due to the riding surface covering the plate; some data were therefore
rejected at the analysis stage because the point of application of the GRF on
the forceplate was within 100 mm of the edge of the plate, indicating that the
entire GRF had not been transmitted through the forceplate. If three or fewer
runs were left after this rejection, we did not calculate mean vertical GRF
and MCP joint angle graphs for that horse/gait. Data are therefore not
reported for lead canter in horses 5, 6 and 7 and non-lead canter for horse
4.
Representative graphs (4 runs) of vertical GRF and MCP joint angle (means ± 1 S.D.) during the stance phases of walk, trot, lead canter, non-lead canter and jump landing are shown in Fig. 5AE. The S.D. values of both variables were small, demonstrating the very repeatable nature of the gaits. The two sets of plots have the same shape during stance and are similar to those reported previously for ridden and riderless locomotion. Peak MCP joint angle occurred 10-20 ms after the vertical GRF peaked. Peak MCP joint angles and mass-specific vertical GRFs increased from walk (216±5° and 6.16±0.53 N kg-1 BM, respectively) to trot (232±4° and 10.73±1.22 N kg-1 BM, respectively) and trot to non-lead canter (238±7° and 11.95±0.66 N kg-1 BM, respectively). The non-lead forelimb at canter experienced a greater peak MCP joint angle and peak vertical GRF than the lead forelimb (228±2° and 9.74±1.40 N kg-1 BM, respectively) (Table 2). The peak values for jump landing were less predictable (234±6° and 10.60±1.27 N kg-1 BM, respectively): in five horses the peak values were similar or lower than those seen at trot, whereas in two horses they were greater than the peak values for the non-lead limb at canter.
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The relationship between MCP joint angle and vertical GRF is shown for one horse at trot in Fig. 6. r2 values for the linear regression lines calculated for the loading and unloading phases of the relationship were all greater than 0.95, showing that there is a very strong positive correlation between MCP joint angle and vertical GRF at all gaits. The mean stiffness of the MCP joint during loading in trot locomotion was 0.29±0.03 N kg-1 deg.-1, range 0.25-0.35 N kg-1 deg.-1 for the seven horses. The mean functional stiffness of the MCP joint during unloading in trot locomotion was 0.27+0.03 N kg-1 deg.-1, range 0.24-0.33 N kg-1 deg.-1. The relationship, and hence distal limb stiffness, was very similar at the different gaits (walk, trot, non-lead canter, lead canter and jump landing) (Fig. 7). The vertical GRFs required to produce an MCP joint angle of 230° were calculated using the linear regression lines for the loading and unloading phases of stance and are shown in Table 2. A single-factor ANOVA showed that there was no gait effect on the calculated vertical GRF for a joint angle of 230° at different gaits. The values for jump landing were, however, more variable than the values for other gaits. There was ±4-11% range around the mean in the calculated values including the values for jump landing, and ±2-7% range around the mean excluding the values for jump landing.
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The values of vertical GRF for a MCP joint angle of 230° were lower for the unloading phase than the loading phase of the relationship at trot (P<0.01), lead canter (P=0.02), non-lead canter (P=0.03) and jump landing (P=0.03) (Table 2).
Fig. 8 shows peak MCP joint angle plotted against peak vertical GRF for each horse in each different gait. Each horse is represented by a different symbol on the graph. The regression lines for each horse show that there is a linear relationship between the two parameters across different gaits (r2=0.90-0.99). A regression for the group of horses shows that a similar relationship exists across a group of horses (r2=0.70, P<0.001).
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(4) Estimation of peak vertical ground reaction force at gallop
Mean vertical GRF and MCP joint angles during the stance phase of trot on a
hard surface for one of the horses are shown in
Fig. 9. Comparison with data
generated on a soft surface (Fig.
5B) demonstrates that the limb loaded more rapidly on the hard
surface but the limb unloaded at a similar rate on both surfaces. As a result
of this, peak vertical GRF and peak MCP joint angle occurred earlier on the
hard surface. The loading portion of both the vertical GRF and MCP joint angle
showed much more high-frequency oscillation on the hard surface
(Fig. 9) than on the soft
surface (Fig. 5B).
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The equations of the linear regression lines calculated for the loading phase of the overground trot data for each horse were used to estimate the vertical GRF required to achieve the peak MCP joint angles recorded at gallop on the treadmill. The left forelimb was the lead forelimb in two horses and the non-lead forelimb in two horses. Data were collected from one horse whilst galloping on both leads. Peak MCP joint angle was 237.6° (range 234°-240.4°) for the lead forelimb and 245.3° (range 241.8°-248.1°) for the non-lead forelimb. Estimated peak vertical GRF at gallop was 12.79 N kg-1 BM (range 12.07-13.73 N kg-1 BM) for the lead forelimb (N=3) and 15.23 N kg-1 BM (13.51-17.10 N kg-1 BM) for the non-lead forelimb (N=3).
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Discussion |
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The determination of length change in the proximal portion of the limb is
less accurate than the distal limb, due to the effect of skin displacement.
The movement of the skin relative to the underlying skeletal landmarks is much
greater in the proximal limb than the distal limb
(van Weeren et al., 1990).
During the stance phase there is 5-10 mm of skin displacement relative to the
proximal spine of the scapula both along the axis of the bone and
perpendicular to it, but there is minimal skin displacement at the elbow joint
(van Weeren et al., 1990
). The
skin displacement perpendicular to the scapula would be expected to have some
influence on the results reported but not sufficient to alter the conclusions
of the paper.
The relationship between MCP joint angle and limb force was similar in
different horses and gaits. This is similar to the results of Farley et al.
(1993) who showed that limb
stiffness does not increase with increasing speed across a range of species.
The stiffness of the limb determines the natural frequency of the spring mass
locomotion model, hence, similar limb stiffness would be predicted as similar
sized horses have similar stride frequencies
(Leach and Cymbaluk, 1986
).
Superficial digital flexor tendon stiffness varies by a factor of two between
different thoroughbred horses (Wilson,
1991
) so the lever arms of the tendons or the stiffness of other
structures must compensate for this. Stance time drops with speed, but the
time required to protract the limb is relatively independent of gait and speed
in the horse (Wilson et al.,
2000
). Whilst the sweep of the limb during stance rises somewhat
(Farley et al., 1993
), this
increase is insufficient to prevent the drop in stance time. The proportion of
time spent in stance (duty factor) therefore drops with speed
(Biewener 1983
;
Pratt and O'Connor, 1978
).
Since average limb force over time must equal body weight this results in an
increase in peak vertical GRF, a greater MCP joint angle and, hence, a greater
compression of the distal limb spring. The only joint with significant
capacity to create length change in the distal limb is the MCP joint. Bone and
tendon strain also rise with speed, presumably due to the increased peak limb
force and increased extension of the MCP joint
(McLaughlin et al., 1996
;
Pratt and O'Connor, 1978
;
Rubin and Lanyon, 1987
;
Stephens et al., 1989
).
The similarity of limb stiffness in different horses also provides an
explanation for the apparent quiescence of energy-storing tendons in response
to changes in mechanical environment
(Wilson, 1991;
Birch et al., 1999
). If a
tendon were to hypertrophy it would be stiffer, which would diminish its
ability to store and return energy at an appropriate rate during the gait
cycle and alter the frequency of the spring mass system.
The slope of the MCP joint anglelimb force relationship was 10%
higher in vitro than in vivo (P<0.01). The
digital flexor muscles originate on the medial epicondyle of the humerus;
thus, the locking of the elbow joint in the in vitro loading system
removed any extensor effect of the digital flexor muscles at the elbow joint.
It is likely that the difference between the in vitro and in
vivo stiffness observed here is due, in part, to the removal of the link
that the elbow joint provides between the distal and proximal springs in
vivo. The elbow gradually extends through stance
(Back et al., 1995), which will
allow the digital flexor muscle bellies to shorten. Much of the load is
transmitted through the accessory ligaments that bypass the muscle and attach
within the distal limb, so this effect will be limited. An additional
contributing factor to the differences between the in vitro and
in vivo plots is the orientation of the limb during in vitro
loading. In vivo at trot the limb sweeps through an angle of
approximately 27° during the loading phase of stance and a similar angle
during the unloading phase, whereas in vitro the limb was orientated
vertically during loading and unloading. A previous study has shown that the
orientation of the limb through the stance phase has a small effect on limb
stiffness (Wilson et al.,
2001b
).
Comparison of Figs 5 and
9 demonstrates that on the soft
surface, limb loading and MCP joint angle rise more slowly than on the hard
surface. The surface acts as a visco-elastic element in series with the
proximal and distal limb springs
(Gerritsen et al., 1995). A
compliant surface therefore reduces the stiffness the spring mass system as a
whole, reducing its resonant frequency and, hence, rate of force rise
(Wilson et al., 2001b
). The
unloading curves are, however, similar on both surfaces. This is because
equestrian surfaces undergo plastic rather than elastic deformation
(Zebarth and Sheard, 1985
),
which appears, mechanically, as a reduced stiffness on loading (i.e. a greater
shortening of the spring system for the rise in GRF from zero at foot-on to
peak force), but because the surface does not `return' there is no concomitant
effect during unloading. The relationship between GRF and MCP joint angle does
not appear to change as a function of surface, which is further evidence for
little or no capacity to tune the distal spring. If a horse tuned its limb for
the surface, as seen in man (Ferris and
Farley, 1997
), then perhaps the limb would be less compliant
during loading on the soft surface but have the same compliance during
unloading on both surfaces, i.e. the hysteresis loop of MCP angle against
vertical GRF would change as a function of surface plasticity. This is not
evident in our data. The viscous nature of the soft surface also accounts for
the more rapid damping of the high frequency vibrations in the GRF curve on
the soft surface (Wilson et al.,
2001b
). The more gradual rise in GRF should also result in an
increase in stance time/duty factor, explaining why horses gallop more slowly
on soft ground.
The in vivo MCP joint anglevertical GRF relationship was
not identical on limb loading and unloading. There are two possible
explanations for this: (1) approximately 7% of elastic strain energy is
dissipated as heat within the tendon rather than returned
(Ker et al., 1981;
Riemersma and Schamhardt,
1985
; Wilson and Goodship,
1994
); (2) the DIP joint and elbow joint extend through stance.
This transfers load to the deep digital flexor tendon via the
accessory ligament and allows the deep digital flexor muscle to shorten (since
the origin of the muscles moves distally as the elbow extends). The accessory
ligament is shorter and stiffer than the muscle belly, so an increase in
muscle-tendon unit and hence limb stiffness will occur.
The linear relationship between MCP joint angle and limb force would be
expected, since tendon is linearly elastic once loaded beyond its toe region
(Riemersma and Schamhardt,
1985) and the moment arm of the tendons on the MCP joint is
relatively independent of joint angle. The MCP joint angle can therefore be
used to predict limb force from kinematic data either by pre-calibration of
the horse of interest using a forceplate during low speed gait or, given the
similarity between horses, from the population average reported here. Direct
measurement of the GRF at gallop is difficult because stride length at gallop
(approximately 6 m; Rooney,
1986
) is much longer than standard forceplates resulting in a
probability of about one in ten that any one foot will strike the forceplate.
Due to the physiological and mechanical stress that high-speed gallop places
on the horse it is very difficult to achieve a sufficient number of forceplate
strikes to provide meaningful data. Force measuring shoes have been used
(Barrey, 1990
;
Kai et al., 1999
;
Ratzlaff et al., 1997
), but
the data is often difficult to relate to the GRF; also they are difficult to
build for reliable measurement on soft surfaces and their mass can interfere
with normal gait, as the horse's foot accelerates at approximately 400 m
s-2 at foot-off (A. M. Wilson, unpublished data). The peak limb
forces predicted here from joint angle data for the non-lead forelimb
(13.51-17.10 N kg-1 BM) are similar to the limited data (one horse)
published elsewhere using direct measurement with a forceplate, which states a
peak vertical GRF of 1.7x body mass
(Kingsbury et al., 1978
).
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Acknowledgments |
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References |
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