Vertical head and trunk movement adaptations of sound horses trotting in a circle on a hard surface

The Veterinary Journal 193 (2012) 73–80

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Vertical head and trunk movement adaptations of sound horses trotting in a circle on a hard surface Sandra D. Starke a,⇑, Egbert Willems b, Stephen A. May c, Thilo Pfau a a

Structure and Motion Laboratory, Department of Veterinary Clinical Sciences, The Royal Veterinary College, Hatfield AL9 7TA, UK Cliffe Equine Clinic, Laughton, E. Sussex BN8 6AJ, UK c Department of Veterinary Clinical Sciences, The Royal Veterinary College, Hatfield AL9 7TA, UK b

a r t i c l e

i n f o

Article history: Accepted 20 October 2011

Keywords: Circle Horse Trot Sound Kinematics

a b s t r a c t Trotting a horse in circles is a standard and important part of the subjective equine lameness examination, yet objective data on this form of locomotion are sparse. The aim of this study was to investigate the effect of trotting in a circle on head and trunk movement symmetry. Vertical movements of the head, withers, os sacrum and left and right tuber coxae were measured using inertial sensors as 12 sound horses were trotted on a hard surface in a straight line and in a circle on both reins. Seven asymmetry measures and hip hike were calculated for each horse for at least nine strides of comparable stride duration across the three conditions (deviation on horse level 63.7% stride duration). Trotting in a circle introduced systematic changes to the movement pattern of all five body landmarks, affecting most asymmetry measures. On average the asymmetry magnitude was comparable for midline locations between reins and for the tuber coxae on opposite reins with few exceptions, although individual horses showed unsystematic differences between the two reins. The results from this study showed that the thresholds for objective discrimination between lame and non-lame horses will need adjustment on the circle due to the observed asymmetry bias. Ó 2011 Elsevier Ltd. All rights reserved.

Introduction Lameness is the most prevalent equine health problem in many countries (Keegan, 2007; Dyson et al., 2008; Egenvall et al., 2009) and has substantial cost and welfare implications (Jeffcott et al., 1982; US Dept. of Agriculture, 2001). Although visual lameness examination has a long tradition, its repeatability has been questioned (for review, see Keegan, 2007) and it is susceptible to observer bias (Arkell et al., 2006). As a result, research into objective lameness detection is becoming increasingly popular (Keegan, 2007). In subjective (Percivall, 1849) and objective gait analysis, a horse is generally classified as unilaterally lame if it displays asymmetry of the midline locations above a certain threshold between the two steps of one, normally symmetrical, trot stride (a stride is defined as touch-down of one limb to the subsequent touch-down of the same limb). Several measures to quantify this movement asymmetry have been proposed based on the ratio of the first and second upward displacement, velocity or acceleration amplitude (Buchner et al., 1996; Uhlir et al., 1997), signal decomposition (Peham et al., 1996; Audigié et al., 2002; Thomsen et al., 2010) ⇑ Corresponding author. Tel.: +44 01707 666425. E-mail address: [email protected] (S.D. Starke). 1090-0233/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tvjl.2011.10.019

and/or differences between movement peaks and troughs (Kramer et al., 2004); these measures are called ‘directional’ if they change in sign when the left or right limb is lame, and ‘non-directional’ if not. Trotting in a circle often exacerbates lameness and, depending on rein and surface properties, provides valuable additional information to the clinician, particularly in cases of bilateral lameness that might otherwise remain undetected (Miller, 1925; Ross, 2002). Kinematic gait analysis is equally unable to detect such symmetrically bilateral lameness conditions on the straight, whereas trotting in a circle will help to facilitate complete objective lameness detection and quantification. To date, the focus of movement analysis during circular trotting has been on centre of mass movement of the head/neck and body (Clayton and Sha, 2006) and the variability of pelvic asymmetry measures on a soft surface (Walker et al., 2010). Recent conference contributions have focused on head and os sacrum asymmetry on a soft circle (Rhodin et al., 2010) and ground reaction forces on different surfaces (Chateau et al., 2011). The aim of the present study was to quantify the effect on vertical head and trunk displacement of trotting in a circle on a hard surface compared to trotting in a straight line. We hypothesised that: (1) due to centripetal force and resulting body lean, circular trotting will introduce systematic asymmetry to the movement

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of non-lame horses; (2) trotting on the left and right rein will induce comparable asymmetry magnitude for midline locations, and (3) the extent of asymmetry of the tuber coxae will be similar on opposite reins (i.e., asymmetry of the left tuber coxae on the left rein and right tuber coxae on the right rein will be comparable).

Data analysis Vertical (aligned with gravity) acceleration was high pass filtered using a fourth order zero-lag Butterworth filter (cut-off frequency 1 Hz) and double integrated to calculate drift-free displacement (Pfau et al., 2005). Vertical displacement of all five sensors was segmented into strides from early stance of the left hind (LH) limb, determined from pelvic roll and a minimum in vertical velocity of the os sacrum. We have validated this stride cutting routine against foot-mounted accelerometers, finding 100% reliability in segmenting data from the correct limb, the velocity minimum occurring at a mean (SD) of 11.4 (0.73)% stride duration after touch down (S.D. Starke, unpublished data). Stride duration was calculated from the segmentation points, and vertical displacement for each stride was interpolated to 101 samples (0–100% stride). To control for trotting speed between conditions, strides were selected from a narrow range of stride durations of each individual horse (preferred stride duration ± max. 40 ms). The following features (for details see Table 2 and Fig. 1) were calculated for each stride and each condition:

Materials and methods This study was granted approval by the Royal Veterinary College (RVC) Ethics Committee.

Horses Twelve sound horses were included after selection from a pool of data from 26 possible candidates (riding school horses, horses belonging to the RVC teaching herd and one horse discharged from the RVC Equine Referral Hospital with no detectable lameness). Horses were considered objectively sound if their movement asymmetry during trot in a straight line was within the mean plus 1 standard deviation (SD) of that of sound horses from previously published data (Buchner et al., 1996; Audigié et al., 2002). This approach used the two asymmetry measures Symmetry Index (SIup), quantifying asymmetry between the two upwards movement amplitudes of one stride, and Energy Ratio (ER), which quantified the general asymmetry of the movement signal. For hind limb lameness, horses were included if 0.17 6 SIup 6 0.17 and ER P 0.9 for vertical os sacrum displacement. For forelimb lameness, horses were included if 0.18 6 SIup 6 0.18 for vertical head displacement and ER P 0.94 for withers displacement due to the absence of ER reference values for the head (compare Table 1 for SIup values of included horses).

1. Symmetry Indices of the upwards (SIup) and downwards (SIdown) amplitudes of the first (Amp1) and second (Amp2) step of the stride (Uhlir et al., 1997):

SIup=down ¼

Ampup=down;1  Ampup=down;2 ; maxfAmpup=down;1 ; Ampup=down;2 g

here based on the vertical displacement instead of acceleration used by Uhlir et al. (1997). 2. Energy Ratio (ER) calculated from the first (A1) and second (A2) harmonic amplitude of the Fourier decomposed movement signal (Audigié et al., 2002):

ER ¼ Equipment

A22 A21

þ A22

:

3. Motion Symmetry (MS) calculated as ER but without squaring the amplitudes (Peham et al., 1996):

Five MTx inertial sensors (Xsens) were attached to the head, withers, os sacrum and left and right tuber coxae (LTC, RTC). These six degree of freedom sensors allow measurement of vertical movement regardless of their orientation on the horse (Pfau et al., 2005). The head sensor was fastened to the highest point on the halter (poll) using a custom built Velcro (Kornbond) attachment and the remaining four trunk mounted sensors were affixed using custom made attachments and crosselastic cohesive foam fixative (Animal Polster). The withers sensor was attached between T4 and T6, although in rare cases it was positioned further caudally (T7/T8) to avoid interference of the mane. Raw data were sampled at 100 Hz per individual sensor channel and transmitted via Bluetooth from an Xbus unit (Xsens), attached to the horse using an elastic surcingle, to a nearby laptop computer.

MS ¼

A2 : A1 þ A2

4. The difference between the two minima (Min_diff) and between the two maxima (Max_diff) of the movement (Kramer et al., 2004):

Min diff ¼ Min1  Min2 Max diff ¼ Max1  Max2 : 5. ‘Peak-to-peak’, reflecting Max_diff normalised to range of movement (RoM) of the horse:

Peak-to-peak ¼ Data collection

Max diff : RoM

6. ‘Hip hike’, defined as the upwards movement amplitude of the LTC before touchdown of the LH (LTC Ampup,2) and upwards movement amplitude of the RTC before touchdown of the RH (RTC Ampup,1). 7. ‘Hip_hike_diff’, the difference between the two ‘hip hike’ amplitudes:

Horses were led in-hand in a straight line (approximately 40–45 m) at least four times to gather a sufficient number of strides that would subsequently allow for selection of strides with similar duration. Horses were lunged in a circle (diameter approximately 10–14 m) on the left and right rein, collecting at least 25 continuous strides. The surface for all conditions was flat and hard, varying between standard Tarmac, non-slip coated Tarmac and roughened concrete.

Hip hike diff ¼ LTC Ampup;2  RTC Ampup;1 :

Table 1 Horse-specific details on number of analysed strides and duration of strides selected for analysis for the three conditions: trotting in a straight line (S) and trotting in a circle on the left and right rein (LR, RR). SIup for head and os sacrum for trotting in a straight line is presented as an indicator of individual baseline asymmetry. Values for stride duration and SIup are given as mean (SD). For stride duration, the percentage difference from the mean stride duration of each horse across all three conditions is indicated in square brackets [ ]. The largest difference from the mean stride duration was 3.7% (horse 9), a minus sign indicating a longer stride duration (and therefore slower speed) compared to the mean. Horse

1 2 3 4 5 6 7 8 9 10 11 12

Number of strides

Stride duration (in ms)

LR

RR

S

LR

20 9 13 21 18 10 12 17 11 18 19 18

15 9 13 15 16 13 20 19 23 18 14 17

21 11 17 10 17 11 19 9 10 24 12 14

735 776 718 712 722 642 656 732 689 620 664 708

SIup during straight trotting RR

(12) (19) (15) (15) (16) (10) (18) (10) (12) (16) (17) (13)

[0.2] [0.6] [0.4] [0.5] [1.0] [2.0] [0.2] [1.8] [3.7] [0.9] [1.0] [0.2]

737 761 712 698 713 638 647 726 662 609 673 715

S (14) (12) (13) (13) (17) (14) (16) (13) (26) (13) (23) (10)

[0.9] [1.7] [0.9] [1.4] [0.5] [1.6] [1.0] [1.4] [0.5] [0.5] [2.6] [1.4]

728 775 716 716 710 609 661 699 642 615 634 695

Head (16) [0.5] (14) [0.9] (15) [0.5] (12) [1.4] (16) [0.5] (15) [3.2] (14) [0.5] (11) [2.8] (13) [3.5] (14) [0.5] (5) [3.6] (9) [1.4]

0.09 0.13 0.04 0.10 0.00 0.10 0.08 0.10 0.06 0.18 0.05 0.14

Os sacrum (0.26) (0.18) (0.26) (0.14) (0.29) (0.35) (0.35) (0.24) (0.18) (0.15) (0.20) (0.17)

0.14 0.11 0.03 0.07 0.10 0.11 0.04 0.08 0.13 0.05 0.06 0.09

(0.11) (0.10) (0.12) (0.08) (0.11) (0.16) (0.13) (0.11) (0.10) (0.10) (0.13) (0.08)

S.D. Starke et al. / The Veterinary Journal 193 (2012) 73–80 Table 2 Details on the calculated asymmetry measures including, for each measure used in this study, full explanation and guides for interpretation. Parameter

Explanation

SIup

Symmetry Index of the upwards movement amplitudes. Directional, non-dimensional relationship between the two upwards movement amplitudes of the two steps of one trot stride A value of ±1 indicates maximum asymmetry (the sign depending on the affected limb) and a value of 0 indicates perfect symmetry

SIdown

Symmetry Index of the downwards movement amplitudes. As SIup, just for the two downwards movement amplitudes of the two steps of one trot stride A value of ±1 indicates maximum asymmetry (the sign depending on the affected limb) and a value of 0 indicates perfect symmetry

ER

Energy Ratio. Non-directional, non-dimensional measure of general asymmetry of a movement signal, derived from signal decomposition. The first harmonic (A1) represents the asymmetric component of the signal, the second harmonic (A2) represents the symmetric component A value of 1 (equivalent to 100%) indicates perfect symmetry, increasing movement asymmetry results in a non-linear decrease in ER due to the squared amplitudes

MS

Motion Symmetry. Non-directional, non-dimensional measure of general asymmetry of a movement signal, derived as ER but without squaring the amplitudes of the harmonics A value of 1 (equivalent to 100%) indicates perfect symmetry, increasing movement asymmetry corresponds to a decrease in MS

Max_diff

Difference between maxima. Directional, metric measure of the difference between the two peaks of the vertical movement signal A value of 0 mm indicates perfect symmetry of the peaks, increasing asymmetry reflected by increasing magnitudes in values

Min_diff

Difference between minima. Directional, metric measure of the difference between the two troughs of the vertical movement signal A value of 0 mm indicates perfect symmetry of the troughs, increasing asymmetry reflected by increasing magnitudes in values

Peak-to-peak

Directional, non-dimensional measure of Max_diff normalised to range of movement (RoM) to allow for direct comparison across horses of different size with different ranges of movement A value of 0 indicates perfect symmetry of the peaks, increasing asymmetry is reflected by increasing magnitudes in values; a value of 1 would indicate that Max_diff = RoM

Hip hike

The upwards movement amplitude of the left tuber coxae (LTC Ampup,2) before touchdown of the left hind leg and the upwards movement amplitude of the right tuber coxae (RTC Ampup,1) before touchdown of the right hind leg In a perfectly symmetrical horse, both movement amplitudes would be exactly the same; with increasing lameness, the movement amplitude of the tuber coxae of the lame limb increases compared to the movement amplitude of the tuber coxae of the sound limb

Hip_hike_diff

Directional, metric measure of the difference between the two hip hike amplitudes (LTC Ampup,2 and RTC Ampup,1) of the tuber coxae A value of 0 indicates perfect symmetry, increasing asymmetry is reflected by increasing magnitude in values. A positive sign indicates left hind lameness (LTC Ampup,2 > RTC Ampup,1) and a negative sign indicates right hind lameness (LTC Ampup,2 < RTC Ampup,1)

Statistical analysis Statistical analysis was carried out in SPSS (Version 18) and data were considered significant for P < 0.05. Data were tested for normality using the Shapiro–Wilk test. To test for the effect of trotting direction on asymmetry measures (hypothesis 1), normally distributed data were compared using a repeated measures ANOVA (Ennos, 2007) and, in case of significance, a pair-wise comparison of the main effect

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was performed (P values Bonferroni corrected). For non-normally distributed data the Friedman test for related samples was performed and, in case of significance, a pair-wise Wilcoxon Signed-Rank Matched Pairs test was performed post hoc, corrected for multiple testing by adjusting the significance level to P < 0.0167 (Field, 2005). Assuming hypothesis 1 was incorrect and the three conditions had no effect on movement (a) symmetry, none of the three pair-wise comparisons should show a difference in magnitude and sign for any measure. To test the magnitude of asymmetry introduced on the left and right rein (hypotheses 2 and 3), the directional asymmetry measures for the left rein were multiplied by 1 and a paired t test (normally distributed data) or Wilcoxon Signed-Rank Matched Pairs test (non-normally distributed data) was performed to compare data for the left and right rein. Tuber coxae data were compared firstly between the inside limbs (left tuber coxae on the left rein versus right tuber coxae on the right rein) and secondly between outside limbs (left tuber coxae on the right rein versus right tuber coxae on the left rein).

Results A mean (SD) of 15 (4) strides were analysed for each horse and each condition. Mean (SD) stride duration was 683 (51) ms for trotting in a straight line (‘straight’ in the following), 698 (45) ms for trotting in a circle on the left and 691 (45) ms on the right rein, respectively (‘left rein’ and ‘right rein’ in the following). Horse-specific details are given in Table 1. Trotting in a circle introduced systematic changes in the vertical movement pattern of all five body landmarks as shown in Fig. 2. Hypothesis 1 (circular trotting introduces systematic asymmetry to the movement of non-lame horses) Results for the seven asymmetry measures of all five body landmarks in the three trotting conditions are shown in Table 3. There was no significant difference between all three conditions in only 7/37 instances; these were SIdown, Max_diff and peak-to-peak of the head (P = 0.862, 0.138 and 0.089), as well as Max_diff and peak-to-peak of the os sacrum (P = 0.197 and 0.178) and RTC (P = 0.096 and 0.059). For the three midline locations, the remaining asymmetry measures were significantly different between all three conditions (P < 0.0001–0.049) except for the following: (a) ER and MS compared between left and right rein (P P 0.096) for all three locations due to their non-directionality; (b) SIup for the withers compared between left and right rein as well as straight and left rein (P P 0.209); and (c) SIup and Min_diff for the head compared between straight and right rein (P P 0.081). No significant difference was detected for ER, Max_diff and peak-to-peak when comparing the outside tuber coxae to the straight (P P 0.262), and for SIdown and Min_diff when comparing the inside tuber coxae to the straight (P P 0.145). However, although the mean values showed a trend towards different magnitudes (compare to Table 3), the variation for tuber coxae was comparatively large between horses and possibly prevented the detection of a significant effect. Further, peak-to-peak and Max_diff were not significantly different between left and right rein for either tuber coxae (P P 0.059). The ‘hip hike’ (amplitude of an individual tuber coxae) was significantly different between straight line and left rein for RTC (P = 0.017) and between right rein and straight line/left rein for LTC (P 6 0.018). Mean (SD) Hip_hike_diff was 15 (15) mm on the left rein, 12 (11) mm on the right rein and 2 (7) mm in a straight line. The average intra-horse variation is presented in Table 4. Hypotheses 2 and 3 (trotting on the left and right rein has a comparable effect for midline locations and for the inside or outside tuber coxae) The magnitude of asymmetry displayed between reins was not significantly different for head, withers and os sacrum

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Fig. 1. Schematic vertical movement pattern of one of the five body landmarks, annotated with key features used in calculating asymmetry measures. Min1 and Min2, first and second minimum; Max1 and Max2, first and second maximum; Ampup,1 and Ampup,2, first and second upwards movement amplitude; Ampdown,1 and Ampdown,2, first and second downwards movement amplitude; Min_diff and Max_diff, difference between the minima and maxima; LH, left hind; LF, left fore; RH, right hind; RF, right fore. Strides are segmented from early stance of the LH, identified from the minimum in vertical velocity (dashed line) and pelvic roll towards the RH. Touch-down of the limbs (indicated by arrows marked as ‘LH on’ and ‘RH on’) corresponds to approximately zero-crossing of the vertical velocity.

Fig. 2. Vertical movement pattern of each of the five body landmarks plotted against percentage stride duration (LTC, left tuber coxae; RTC, right tuber coxae). Mean ± SD for 12 non-lame horses are shown for each condition. Black dashed (mean) and dotted (SD) lines: trotting in a straight line; red solid line (mean) and shading (SD): trotting in a circle on the right rein; blue solid line (mean) and shading (SD): trotting in a circle on the left rein. For the three pelvis locations, approximate touch-down events of the hind limbs and for head and withers, approximate touch-down events of the forelimbs are identified with arrows. LH, left hind; RF, right fore; RH, right hind; LF, left fore.

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Table 3 Mean (SD) for seven asymmetry measures (n = 12) of all five body landmarks and hip hike as well as median [inter-quartile range] exclusively for non-parametric datasets (presented if data for at least one of the conditions were non-normally distributed). The table shows that trotting in a circle resulted in a change in value and/or sign for most asymmetry measures on most locations between the three conditions: for locations along the midline of the horse (head, withers and os sacrum), values moved from high symmetry during trotting in a straight line towards lower symmetry during trotting in a circle, the sign depending on the rein for the directional measures. For the tuber coxae, the three conditions caused changes in symmetry as well, although moving towards both, increased or decreased symmetry, depending on the rein and condition. Asymmetry measure

Rein

Head

Withers

LTC

Os sacrum

RTC

SIup

LR RR S

0.27 (0.25)s,r 0.19 (0.34)l 0.00 (0.10)l

0.06 (0.12) 0.06 (0.13)s 0.05 (0.07)r

0.39 (0.09)r 0.10 (0.15)s,l 0.27 (0.10)r

0.23 (0.18)s,r 0.25 (0.16)s,l 0.02 (0.09)l,r

0.07 (0.22)s,r 0.39 (0.14)s,l 0.21 (0.14)l,r

SIdown

LR

0.06 0.07 0.14 0.23 0.05 0.02

(0.26) [0.32] (0.26) [0.50] (0.12) [0.09]a

0.25 (0.16)s,r

0.08 (0.15)r

0.10 (0.12)s,r

0.04 (0.16)s,r

0.31 (0.10)s,l

0.08 (0.15)s,l

0.23 (0.18)s,l

0.10 (0.17)l

0.03 (0.07)l,r

0.10 (0.06)r

0.01 (0.09)l,r

0.05 (0.15)l

0.78 0.77 0.75 0.77 0.92 0.95

(0.10) [0.09]S (0.14) [0.13]S (0.06) [0.07]a,L,R

0.90 0.96 0.89 0.90 0.98 0.99

(0.09) [0.16]a,S (0.06) [0.08]S (0.01) [0.01]L,R

0.88 (0.07)s

0.90 0.90 0.86 0.88 0.98 0.97

0.91 0.91 0.83 0.85 0.93 0.93

0.69 0.67 0.67 0.68 0.80 0.83

(0.08) [0.06]a,S (0.10) [0.11]S (0.06) [0.07]a,L,R

0.78 0.84 0.76 0.76 0.90 0.91

(0.09) [0.16]a,S (0.06) [0.07]S (0.03) [0.05]L,R

0.75 0.76 0.82 0.82 0.80 0.81

RR S ER

LR RR S

MS

LR RR S

Max_diff (in mm)

LR RR S

Min_diff (in mm)

Peak-to-peak

Hip hike (in mm)

9 (13) 14 [18]a 3 (16) 2 [18] 1 (5) 0 [8]

0.94 (0.03) 0.94 (0.03)l

(0.06) [0.08]S (0.09) [0.15]S (0.01) [0.01]a,L,R

(0.04) [0.06]R (0.10) [0.12]S,L (0.04) [0.04]a,R

0.78 (0.06)S

0.79 (0.05)R

0.75 (0.08)S

0.71 (0.08)S,L

0.88 (0.02)L,R

0.79 (0.05)R

12 (4)s

4 (8)

6 (7)

0 (5)

1 (3)l,r

7 (6)l

2 (5)

4 (12) 2 [10]a 11 (9) 10 [13] 6 (10) 4 [13]

12 (6) 12 [7]S,R 14 (9) 16 [12]S,L 1 (2) 0 [2]a,L,R

2 (8)s,r

0.05 (0.15) 0.02 [0.13]a 0.13 (0.12) 0.14 [0.14] 0.07 (0.13) 0.05 [0.18]

11 (6)s,r 13 (5)

s,l

(0.07) [0.10]a (0.04) [0.06] (0.04) [0.04]

LR

8 (12)s,r

7 (8)s,r

21 (10)r

RR

14 (16)l

10 (7)s,l

2 (10)s,l

S

1 (4)l

3 (4)l,r

17 (6)r

LR

0.16 (0.20)

0.16 (0.10)s,r

0.14 (0.06)s

0.06 (0.11)

RR

0.03 (0.21)

0.19 (0.08)s,l

0.09 (0.09)

0.00 (0.07)

S

0.01 (0.08)

0.01 (0.04)

LR RR S

– – –

– – –

l,r

l

0.08 (0.06)

0.02 (0.08)

83 (17)r 66 (16)s,l 83 (19)r

– – –

20 (8)l 12 (6)l

68 (15)s 79 (17) 81 (16)l

Refer to Table 1 and Table 2 for abbreviations. aThis set of measurements was not normally distributed; s.l.r., significantly different result (parametric test) compared to straight line (s), left rein (l) and right rein (r), respectively; S.L.R., significantly different result (non-parametric test) compared to straight line (S), left rein (L) and right rein (R), respectively.

(P = 0.057–0.976) and for the inside or outside tuber coxae (P = 0.135–0.970), except for SIdown of the head (P = 0.021) and ER of the tuber coxae on the outside of the circle (P = 0.038). Consequently, the overall mean/median difference between left and right rein for most asymmetry measures was very small for all five body landmarks (Table 5). However, there was considerable variation on the individual level, as reflected in large standard deviation/interquartile range (Table 5), particularly for the head. Discussion In this study we have quantified the effect of trotting in a circle on a hard surface on vertical head and trunk movement symmetry. The results relating to hypothesis 1 showed that the majority of asymmetry measures were systematically biased during trot in a circle (Table 3). In order to objectively discriminate between non-lame and lame horses on the circle, thresholds for these

measures therefore need to be adjusted to avoid incorrectly declaring the limb on the inside of the circle as lame. It is possible that circle diameter (Clayton and Sha, 2006) and trotting speed influence the amount of systematic asymmetry and stride consistency (Peham et al., 1998), therefore such adjustments may not be universally applicable and it would be valuable to quantify the effect of these parameters on movement asymmetry. Adjustments may, however, not be necessary if asymmetry measures are not significantly affected, which could prove a robust way to determine lameness if these asymmetry measures are sensitive to lameness and reliable in indicating the lame limb. For the partially non-significant results, the combination of relatively small sample size (n = 12), observed inter-horse variation and conservative correction for multiple testing might have resulted in a type-II error (declared non-significant despite being significant). This was most likely in cases where trotting in a circle on only one rein was significantly different from trotting in a

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Four measures (Max_diff, Min_diff, hip hike and Hip_hike_diff) were absolute measures of displacement that were likely to vary with horse size. The study population covered pony to Warmblood (approximate withers height of 1.3–1.7 m) and reflected a crosssection of horses commonly seen in equine practice. However, at the extremes of the size range, horse size might have to be taken into account when discriminating between soundness and lameness using the results presented here. Normalising Max_diff to range of movement (‘peak-to-peak’) showed the same statistical response as the absolute parameter. However, since the range of movement is likely to change with severity of lameness, such normalised parameters may lose detail of the actual changes in asymmetry, especially for mild lameness. Trotting in a circle introduced two movement features that would subjectively indicate lameness during trotting in a straight line: the tuber coxae on the inside of the circle showed a mild increased hiking movement (reflected in Hip_hike_diff – 0) and the head showed a mild nod-down during stance of the outside forelimb, corresponding to ‘lameness’ of the inside fore- and hind limb when judged according to subjective criteria on the straight. A systematic asymmetry bias during lunging on a hard surface, which does not constitute lameness, has also been reported to be apparent visually (R.K. Smith, personal communication). It therefore seems likely that the changes measured here are perceivable by expert veterinarians. The results relating to hypotheses 2 and 3 showed that the overall movement asymmetry of locations along the midline as well as of the tuber coxae on opposite reins (comparison of both inside tuber coxae and both outside tuber coxae) was comparable between reins with only two exceptions (Table 5), although there was un-systematic variation at the individual horse level (Tables 4 and 5). Possible explanations for this individual variation were: (1) mild, undiscovered lameness conditions of individual horses exacerbated on the circle and depending on the rein; (2) handedness of individual horses, resulting in differing asymmetry on left and right rein; or (3) variation in circle diameter between the two reins. There was no apparent reason for the significantly different SIdown of the head. The difference between ER of the outside tuber coxae might have resulted from the ER showing an increased, non-linear response to asymmetry (Walker et al., 2010), which might have translated into an over-amplified drop in ER for individual cases. In contrast to Walker et al. (2010), the percentage reconstruction (PR) was high and comparable between straight and circle for os sacrum (PR P 99.11 ± 0.45%), tuber coxae

Table 4 Average intra-horse variation (standard deviation on the horse-level) for seven asymmetry measures of all five body landmarks as well as hip hike of the tuber coxae. Average intra-horse variation was highest for the head but comparable for the other body landmarks and tended to be higher for trotting in a circle than trotting in a straight line. Head

Withers

LTC

Os sacrum

RTC

SIup

LR RR S

0.25 0.27 0.23

0.14 0.15 0.10

0.12 0.16 0.08

0.13 0.17 0.11

0.13 0.16 0.11

SIdown

LR RR S

0.25 0.25 0.21

0.14 0.15 0.10

0.16 0.17 0.14

0.19 0.20 0.11

0.17 0.20 0.10

ER

LR RR S

0.15 0.16 0.06

0.06 0.06 0.01

0.06 0.05 0.03

0.06 0.09 0.02

0.07 0.09 0.03

MS

LR RR S

0.12 0.12 0.08

0.07 0.06 0.05

0.06 0.07 0.05

0.06 0.08 0.06

0.07 0.08 0.05

Max_diff (in mm)

LR RR S

10 11 8

6 6 4

7 7 5

6 6 5

8 8 6

Min_diff (in mm)

LR RR S

11 14 9

6 6 5

7 7 5

6 7 4

7 9 6

Peak-to-peak

LR RR S

0.16 0.16 0.14

0.08 0.09 0.06

0.09 0.10 0.07

0.10 0.10 0.07

0.10 0.10 0.07

Hip hike (in mm)

LR RR S

– – –

– – –

8 8 5

– – –

8 8 6

Refer to Table 1 and Table 2 for abbreviations.

straight line or results for left and right tuber coxae were noncoherent. Where all three conditions were not significantly different for head and os sacrum, we estimated the possible effect size supported by our data from the confidence intervals of effect size (Colegrave and Ruxton, 2003). We found narrow confidence intervals for effect size for Max_diff and peak-to-peak of the os sacrum and wide, partially skewed confidence intervals for Max_diff, peakto-peak and SIdown of the head. For a larger sample, we would therefore expect a small, possibly not biologically relevant, effect size for Max_diff and peak-to-peak of the os sacrum and a larger, possibly biologically relevant, effect size for Max_diff, peak-topeak and SIdown of the head.

Table 5 Difference between asymmetry magnitude displayed by horses when trotting in a circle on the left and right rein for all five body locations and seven asymmetry measures. The directional asymmetry measures for the left rein were negated to compare data without directional effects for the left and right rein, since all data were cut into strides from early stance of the left hind limb. Tuber coxae (TC) data were compared firstly between both inside limbs and secondly both outside limbs. Differences were calculated as left rein minus right rein for each horse and averaged for each measure and location. Values are presented as mean (SD) as well as median (inter-quartile range). The table shows that across horses, there was no systematic difference in asymmetry for most measures and locations (mean difference close to zero). Individual horses, however, showed unsystematic differences between asymmetry magnitude displayed on the left and right rein, reflected in the large standard deviation across all horses. Location

SIup

SIdown

Max_diff

Min_diff

Peak-to-peak

Head

Mean (SD) Median (IQR)

0.08 (0.37) 0.07 (0.26)

0.20 (0.27) 0.19 (0.24)

0.02 (0.15) 0.06 (0.22)

0.02 (0.11) 0.04 (0.17)

6 (14) 6 (18)

6 (18) 2 (22)

0.13 (0.21) 0.12 (0.24)

Withers

Mean (SD) Median (IQR)

0.00 (0.16) 0.02 (0.15)

0.06 (0.12) 0.04 (0.20)

0.01 (0.05) 0.01 (0.05)

0.03 (0.05) 0.01 (0.07)

2 (7) 4 (11)

3 (7) 2 (9)

0.03 (0.10) 0.07 (0.16)

Os sacrum

Mean (SD) Median (IQR)

0.01 (0.21) 0.02 (0.27)

0.13 (0.24) 0.16 (0.29)

0.04 (0.10) 0.02 (0.11)

0.03 (0.10) 0.02 (0.08)

4 (9) 6 (13)

3 (11) 1 (17)

0.06 (0.14) 0.08 (0.22)

Inside TC

Mean (SD) Median (IQR)

0.00 (0.15) 0.02 (0.16)

0.02 (0.21) 0.01 (0.20)

0.05 (0.11) 0.03 (0.12)

0.04 (0.10) 0.02 (0.09)

1 (10) 5 (14)

1 (11) 3 (17)

0.01 (0.12) 0.03 (0.15)

Outside TC

Mean (SD) Median (IQR)

0.03 (0.19) 0.05 (0.16)

0.04 (0.20) 0.01 (0.21)

0.02 (0.04) 0.02 (0.04)

0.03 (0.05) 0.04 (0.05)

2 (10) 2 (12)

0 (11) 3 (17)

0.04 (0.12) 0.02 (0.17)

Refer to Table 1 and Table 2 for abbreviations.

ER

MS

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(PR P 96.87 ± 0.72%), head (PR P 98.02 ± 1.36%) and withers (PR P 97.71 ± 1.53%). At least two mechanisms may be at work that could explain the increase in movement asymmetry of horses trotting in a circle. Firstly, a horse’s response to trotting in a circle may be similar to its response to lameness on the straight, counteracting uncomfortable limb loading with asymmetrical movement to redistribute and/or even out limb loading. This hypothesis was supported by studies on trotters racing over insufficiently banked bends, where an increased strain on particularly the fetlock region of the inside limbs was found using thermographic imaging (Fredricson et al., 1975a). This led to surfaces being banked for trotter races in Sweden following recommendations to reduce unequal loading of limbs (Fredricson et al., 1975a,b). Similarly, lunging on banked surfaces resulted in more ‘normal’ limb posture than lunging on flat surfaces (Hobbs et al., 2011) and the vertical impulse was not significantly different between the inside and the outside limb for horses lunged on a hard, flat surface (Chateau et al., 2011). The second potential reason for asymmetry is that when horses lean into the circle (Clayton and Sha, 2006), asymmetrical movement may be necessary to achieve ground clearance during swing of the inside hind limb by increasing the upwards hike of the inside tuber coxae. Our study supported this hypothesis as well since there was an increase in movement asymmetry and hip hike of the tuber coxae on the inside of the circle. Similarly, asymmetry in head and withers movement may support swinging the front limbs differently on the inside and outside of the circle. Future work will be necessary to test these hypotheses and develop a more comprehensive understanding of the mechanisms causing horses to move asymmetrically on the circle. In the present study, we investigated vertical movement (aligned with gravity). An alternative may be to analyse true dorsoventral movement (in the horse’s sagittal plane), which will deviate from vertical movement on the circle due to observed body lean (Clayton and Sha, 2006). Since a comprehensive understanding of full body dynamics on the circle is lacking, we aimed to avoid additional variation (within and between horses) caused by a change of body lean that may vary with speed and circle diameter. It is not known whether veterinarians assess the movement of the horse on a circle using a horse-based (dorsoventral) or worldbased (vertical) reference frame. We used stride duration as an approximation for trotting speed, since the methodology did not allow direct speed quantification. Within horses, we found a maximum deviation from the horse’s average stride duration by only up to 24 ms (equating to 3.7% stride duration; Table 1). Across horses, the SD ranged from 45 to 51 ms, depending on conditions. To establish an approximation for the magnitude of and potential variation in speed within and across horses, we used published regression data relating stride duration (respectively stride frequency) and speed for a 680 kg horse (Table 1 from Heglund and Taylor (1988)) and calculated the predicted speed for each horse in each condition, arriving at a maximum speed difference from the mean of 6.3%. Across horses, the predicted mean (SD) speed was 3.4 (0.5) m/s for the straight line (range: 2.6–4.1 m/s), 3.3 (0.4) m/s for the left rein (range: 2.6–4.0 m/s) and 3.3 (0.4) m/s for the right rein (range: 2.8– 4.1 m/s). However, since regression equations are influenced by body size and had been established for trot in a straight line, our calculations for magnitude and variation in speed are approximations only. Our horses were allowed to trot at their preferred speed to gain ‘normal’ data for ‘normal’ horses for the given circle diameter range. Future studies will need to establish a link between stride duration and speed on the circle; in case of a different relationship between the two measures on the circle compared to the straight, the scientific community will have to decide which parameter to keep constant in comparative studies.

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Variation in stride duration/trotting speed within and across horses may have contributed to the observed variation in movement asymmetry. However, the variation encountered in this study was comparable to other overground studies using a similar repeated measures design. Keegan et al. (1998) reported a SD for stride duration of 44–55 ms across horses and a maximum difference in mean stride duration of 4 ms between conditions. Galisteo et al. (1997) reported a SD for stride duration of 30 ms and for velocity of 0.2–0.7 m/s, with a maximum difference in mean stride duration between conditions of 10 ms and in mean velocity of 0.05 m/s. Circle diameter could not be tightly controlled, since horses showed different preferences for trotting diameter and handlers had to be varied across yards. Asymmetry was likely to be affected by circle diameter, with largest asymmetry being expected for the smallest diameter (Clayton and Sha, 2006) due to increased centripetal acceleration and resultant body lean. We therefore assumed that variation in circle diameter will have contributed to the observed variation in movement asymmetry across horses and to a lesser degree between left and right rein, since the same handler lunged a horse on both reins. Due to different locations in which horses were situated, surface properties varied between standard Tarmac, non-slip coated Tarmac and roughened concrete. All these surfaces were fully noncompliant, although there may have been slight differences in the coefficient of friction between sites, which may have introduced part of the variation observed between horses; e.g. static and dynamic coefficient of friction for barefoot horses on concrete and HL3 grade asphalt have been found to be different by approximately 0.1 (McClinchey et al., 2004). In comparison, the difference between extreme conditions (hooves on smooth rubber and on steel) would result in a fivefold higher difference of 0.5 (McClinchey et al., 2004). Since a larger number of uncontrollable parameters could vary on the circle (un-discovered exacerbated lameness, (exacerbated) handedness, circle diameter, etc.) than on the straight line, the interaction between these factors may be the reason for the observed larger variation in asymmetry within and across horses on the circle compared to the straight line (Tables 3 and 4).

Conclusions This study has shown that trotting in a circle introduces a systematic bias to the vertical movement symmetry of sound horses. Thresholds for soundness that have been established for trotting in a straight line will therefore need adjustment when objectively assessing horses on the circle. SIdown, Max_diff and peak-to-peak of the head, as well as Max_diff and peak-to-peak of the os sacrum, were the only parameters that consistently did not show a significant difference between the three trotting conditions, although future studies with larger sample sizes may detect a significant effect. While the magnitude of movement asymmetry on the circle was comparable between reins across horses, individual horses showed un-systematic variation between reins; further work will need to establish whether such variation is always indicative of lameness or may reflect handedness. With the present study, we provided the first reference data for ‘normal’ movement that can be expected for sound horses trotting in a circle on a hard surface. In the absence of a gold standard of what is definitely sound, there is the possibility that lameness components may have contributed to the variation observed across horses. In the future, it will be of utmost importance to investigate the effect of speed and circle diameter on systematic asymmetry bias. Further, it will be valuable to establish baseline data on a larger scale, on different surfaces and compare horses that perform in different disciplines to

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establish a better understanding of movement asymmetry in relation to the use of the horse. Conflict of interest statement None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper. Acknowledgements The authors would like to thank Holly Laura Buchan, Rachel Marie-Anne Ashley Smith and Kirsty Raistrick for help with the data collection, two anonymous reviewers for their helpful comments which led to improvement of the manuscript and Thomas Witte for insightful comments on the original manuscript. S.D. Starke is funded through a PhD studentship by the Royal Veterinary College, UK. References Arkell, M., Archer, R.M., Guitian, F.J., May, S.A., 2006. Evidence of bias affecting the interpretation of the results of local anaesthetic nerve blocks when assessing lameness in horses. The Veterinary Record 159, 346–348. Audigié, F., Pourcelot, P., Degueurce, C., Geiger, D., Denoix, J.M., 2002. Fourier analysis of trunk displacements: A method to identify the lame limb in trotting horses. Journal of Biomechanics 35, 1173–1182. Buchner, H.H., Savelberg, H.H., Schamhardt, H.C., Barneveld, A., 1996. Head and trunk movement adaptations in horses with experimentally induced fore- or hindlimb lameness. Equine Veterinary Journal 28, 71–76. Clayton, H.M., Sha, D.H., 2006. Head and body centre of mass movement in horses trotting on a circular path. Equine Veterinary Journal Suppl. 36, 462–467. Colegrave, N., Ruxton, G.D., 2003. Confidence intervals are a more useful complement to nonsignificant tests than are power calculations. Behavioral Ecology 14, 446–450. Chateau, H., Robin, D., Camus, M., Holden, L., Falala, S., Ravary, B., Denoix, J.-M., Pourcelot, P., Crevier-Denoix, N., 2011. Use of a 3D dynamometric horseshoe for the measurement of ground reaction force and moments in horses trotting on right and left circles on different surfaces. In: Conference of the International Society of Biomechanics (ISB 2011), Abstract 624. Dyson, P.K., Jackson, B.F., Pfeiffer, D.U., Price, J.S., 2008. Days lost from training by two- and three-year-old Thoroughbred horses: A survey of seven UK training yards. Equine Veterinary Journal 40, 650–657. Egenvall, A., Lönnell, C., Roepstorff, L., 2009. Analysis of morbidity and mortality data in riding school horses, with special regard to locomotor problems. Preventive Veterinary Medicine 88, 193–204. Ennos, R., 2007. Statistical and Data Handling Skills in Biology. Pearson Education Limited, Harlow, UK, pp. 55–60. Field, A., 2005. Discovering Statistics using SPSS. Saunders, London, UK, pp. 563– 565. Fredricson, I., Dalin, G., Drevemo, S., Hjertén, G., Nilsson, G., Alm, L.O., 1975a. Ergonomic aspects of poor racetrack design. Equine Veterinary Journal 7, 63–65.

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