The effect of trotting speed on the evaluation of subtle lameness in horses

The Veterinary Journal 197 (2013) 245–252

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The effect of trotting speed on the evaluation of subtle lameness in horses Sandra D. Starke a,b,⇑, Kirsty J. Raistrick a, Stephen A. May a, Thilo Pfau a,b a b

Department of Veterinary Clinical Sciences, The Royal Veterinary College, North Mymms, Hatfield AL9 7TA, UK Structure and Motion Laboratory, The Royal Veterinary College, North Mymms, Hatfield AL9 7TA, UK

a r t i c l e

i n f o

Article history: Accepted 1 March 2013

Keywords: Horse Lameness Speed Gait analysis Trot

a b s t r a c t Equine lameness is a significant and challenging part of a veterinarian’s workload, with subtle lameness inherently difficult to assess. This study investigated the influence of trotting speed on perceived and measured changes in movement asymmetry. Ten sound to mildly lame horses were trotted at a ‘slow’, ‘preferred’ and ‘fast’ speed on a hard surface, both on a straight line and in a circle on left and right reins. Video recordings of the horses were visually assessed by six experienced equine clinicians. Vertical movement of head, withers and pelvis was derived from inertial sensor data and several features calculated. On the straight line, more horses were subjectively declared sound at higher speeds, whilst different objective asymmetry measures showed only slight and inconsistent changes. On the circle, speed had no significant effect on the subjective assessment, with an increase in objectively measured asymmetry at higher speeds possibly balanced by a decrease in sensitivity of the observers for this asymmetry. Horses visually examined for subtle lameness on the straight should therefore be evaluated at a slow speed. Trotting speed should be consistent on repeated occasions, especially during objective gait analysis on the circle, to avoid the interaction of treatment effects and speed effects. Ó 2013 Elsevier Ltd. All rights reserved.

Introduction Lameness is the most frequent equine health issue, affecting approximately 11% of horses in the UK (Blue Cross, 2011). The associated cost, welfare and training implications have long been highlighted (Jeffcott et al., 1982; Kaneene et al., 1997; Vigre et al., 2002; Keegan, 2007; Dyson et al., 2008; Egenvall et al., 2009). Correctly detecting the onset of lameness is essential for early intervention, with treatment of lameness increasing the prospect of recovery (Ross et al., 1999). Although a controlled study in horses is currently lacking, early lameness detection and treatment in dairy cows resulted in reduced disease severity, fewer additional treatments and lower lameness prevalence compared to controls (Leach et al., 2012). Despite the impact of lameness on the use and welfare of horses, subtle lameness is inherently difficult to quantify; visual assessment is often less sensitive than technology (McCracken et al., 2012) while being confounded by observer disagreement (Keegan et al., 1998, 2010) and bias (Arkell et al., 2006). Further, the human visual system has limitations in detecting changes (Holcombe, 2009) and the magnitude of perceivable asymmetry is likely restricted (Parkes et al., 2009). Limited tools are available to the clinician for determining subtle gait irregularities in a clinical setting. Attaching visual aids such ⇑ Corresponding author at: Department of Veterinary Clinical Sciences, The Royal Veterinary College, North Mymms, Hatfield AL9 7TA, UK. Tel.: +44 1707 666425. E-mail address: [email protected] (S.D. Starke). 1090-0233/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tvjl.2013.03.006

as white tape to both sides of the pelvis can help make subtle hind limb asymmetry more obvious to the eye (May and Wyn-Jones, 1987; Wyn-Jones, 1988). To exacerbate lameness, horses are commonly lunged on a hard and soft surface (Wyn-Jones, 1988; Baxter and Stashak, 2011; Ross, 2011a) and evaluated after provocation tests such as limb flexion (Wyn-Jones, 1988; Baxter and Stashak, 2011; Ross, 2011b). However, circling introduces speed and diameter-dependent movement adaptations and asymmetry even in sound horses (Clayton and Sha, 2006; Hobbs et al., 2011; Starke et al., 2012a; Pfau et al., 2012) and flexion tests are prone to ‘false positives’ (Wyn-Jones, 1988; Ramey, 1997; Verschooten and Verbeeck, 1997; Busschers and Van Weeren, 2001; Baxter and Stashak, 2011; Ross, 2011b; Starke et al., 2012c). Further tests such as ridden exercises (Baxter and Stashak, 2011; Ross, 2011a) can suffer from the influence of the rider on the gait (Wyn-Jones, 1988; Licka et al., 2004). Trotting speed is one of the parameters that can vary, either intentionally or unintentionally, during the gait examination. Textbooks generally recommend to trot the horse ‘as slowly as practical’ (Baxter and Stashak, 2011), ‘slow’ (Wyn-Jones, 1988) or ‘at a consistent speed, not too slow and too fast’ (Ross, 2011a). While higher speeds often exacerbate prominent baseline lameness (Peham et al., 2000; Chateau et al., 2007), sound and subtly lame horses do not show this systematic change for moderate speed ranges (Peham et al., 1998, 2000; Halling Thomsen et al., 2010). However, since movement pattern inconsistency may cause disagreement between observers (Wren et al., 2005), consistency being greatest at the ‘preferred’ or faster speeds in horses on the

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Fig. 1. Sketch of the monitor setup for subjective grading. Three adjacent monitors showed the same horse during ‘slow’, ‘preferred’ (pref) and ‘fast’ trot either in a straight line, on the left rein or on the right rein. The three clips were randomly distributed between the three monitors.

treadmill (Peham et al., 1998), it could be advisable to select a normal to fast trot when evaluating horses with subtle lameness. To date, this relationship has not been tested. Trotting speed affects most movement features even in sound horses; examples are stride frequency/duration, stance time and stride length (Leach and Drevemo, 1991; Van Weeren et al., 1993; Clayton, 1994; McLaughlin et al., 1996; Galisteo et al., 1998), limb angles (Van Weeren et al., 1993; Clayton, 1994; Galisteo et al., 1998), trunk flexion angles (Robert et al., 2001), features of ground reaction force and impulse (Barr et al., 1995; McLaughlin et al., 1996; Dutto et al., 2004; Weishaupt et al., 2010) as well as muscle activation (Robert et al., 2002). While sound horses show a repeatable ‘preferred’ trotting speed when led by the same handler (Degueurce et al., 1997; Galisteo et al., 1998), lame horses tend to increase their speed after successful local analgesia or surgery (Peham et al., 2000). Especially when re-examining a horse after intrasynovial and perineural analgesia, treatment or prolonged time intervals, it is therefore crucial to keep the trotting speed consistent for reproducible results (Peham et al., 2000; Dyson, 2011; Ross, 2011a) and avoid the interaction of treatment effects and speed effects. The aim of this study was to compare the effect of trotting speed on subjective lameness scores and objective measurements in a group of sound to mildly lame horses on the straight and circle.

Materials and methods Horses and instrumentation This study was granted approval by the Royal Veterinary College (RVC) Ethics Committee. Ten unridden horses belonging to the RVC’s teaching herd with a mean (SD) age of 9 (3) years, mean (SD) body mass of 483 (56) kg, mean (SD) height at the withers of 1.41 (0.12) m and mean (SD) height at the hip joint of 1.26 (0.17) m were used. Horses were instrumented with five MTx inertial sensors (Xsens). These were attached over withers, sacrum and left and right tuber coxae using custom built pouches and Animal Polster (Snøgg) and over the poll using a custom made Velcro (Kornbond) attachment. Sensor data were collected at 100 Hz per individual sensor channel and transmitted via Bluetooth from an Xbus unit (Xsens), attached to a surcingle, to a nearby laptop computer. A GPS logger (Trine II, BTGPS) sampled speed at 1 Hz. GPS data were downloaded (CruxLog software) after each session for further processing.

Data collection Horses were trotted in a straight line (approximately 45 m) and in a circle on the left and right rein (radius approximately 5–6 m) in randomised order at their ‘preferred’ trotting speed as well as a ‘slow’ and ‘fast’ trot determined by the handler. The surface was hard and level throughout, coated with non-slip tarmac. Video recordings (Sony HDR-HC7) were taken during data collection.

Fig. 2. Mean ± SEM number of horses declared sound at the three different trotting speed categories (‘slow’, ‘preferred’ and ‘fast’) across the six assessors. Green (checked), trot on a straight line; blue (striped), trot in a circle on the left rein; red (dotted), trot in a circle on the right rein.

Subjective assessment of lameness For each horse, video clips showing the strides that matched objective analysis (see below) were created in Pinnacle Studio Pro (Pinnacle Systems). For each horse, three video series were created (‘straight line’, ‘left rein’ and ‘right rein’). Each series contained three clips showing the horse trotting at the ‘slow’, ‘preferred’ and ‘fast’ speed (Fig. 1). The three clips of each series were randomly distributed between three adjacent, colour-calibrated (SpiderElite 3, Datacolour) 17 in. (43 cm) monitors (Dell, model E172FPt) and looped simultaneously using Windows Media Player (Microsoft). The order of the thirty video series was randomised per participant. Six experienced veterinarians (on average 11.4 years of experience in assessing lameness, four participants having diplomate status) evaluated each video series for as long as desired, noting down the presence of lame limb(s) and the corresponding lameness score. The 11-point UK scale (Wyn-Jones, 1988; Dyson, 2011) ranging from 0 (sound) to 10 (non-weight bearing lame) was used for grading. After completion of the study, participants were asked to rank the difficulty in assessing lameness at the three speeds. The number of horses declared sound and the average assigned lameness scores to forelimbs and hind limbs during ‘slow’, ‘preferred’ and ‘fast’ trot were compared using a Friedman test (PASW Statistics 18; SPSS). Inter-observer agreement was calculated using the free marginal multirater kappa (Brennan and Prediger, 1981; Randolph, 2005; Warrens, 2010) using an online kappa (j) calculator.1 Objective asymmetry quantification Vertical (=aligned with gravity) acceleration of each inertial sensor was doubleintegrated and highpass filtered (cut-off frequency 1 Hz) to determine drift-free displacement (Pfau et al., 2005). Data were segmented into strides from early stance of the left hind limb (Starke et al., 2012b). Segmentation points were used to calculate stride frequency. For each horse, forty strides were used for trot in a straight line and 25 strides for trot on each rein. The following measures (compare references below and see Starke et al., 2012a, for details) were calculated from the vertical displacement of each stride: Symmetry indices (Uhlir et al., 1997): 1

See: http://justusrandolph.net/kappa.

S.D. Starke et al. / The Veterinary Journal 197 (2013) 245–252

SIup=down ¼

Ampup;1  Ampup;2 : maxfAmpup;1 ; Ampup;2 g

The difference between the two minima and the two maxima (Kramer et al., 2004):

Min diff ¼ Min1  Min2 and Max diff ¼ Max1  Max2 : Vector sum (VS) of minima and maxima (Keegan et al., 2012) was calculated firstly non-directionally as:

VSunsigned ¼

qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi 2 2 Min diff þ Max diff

and secondly directionally (VSsigned) by assigning a negative sign to VS if Min,1 6 Min,2 and a positive sign if Min,1 > Min,2; this calculation attributes asymmetry to the limb on which the head is not nodding down for each individual stride. Features derived from Fourier decomposition (Peham et al., 1996; Audigie et al., 2002) were calculated using the first harmonic amplitude A1 (asymmetric component), the second harmonic amplitude A2 (symmetric component) and motion symmetry MS (Peham et al., 1996):

MS ¼

A2 A1 þ A2

Hip_hike_diff (Starke et al., 2012a) was calculated as:

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Mean values were calculated across all strides per horse except for VSsigned, where median values were calculated since data can show a bimodal distribution. The sign was then removed from these mean/median values for directional measures (SIup,down, Min_diff, Max_diff, VSsigned and Hip_hike_diff) to remove the influence of the left or right limb being lame; these measures are indexed as ‘abs’ below. Vector sum (VS), both signed and unsigned, was chosen to compare subjective and objective assessment of the horses between the three trotting speed categories as it captures all asymmetry components (Keegan et al., 2012). To examine speed effects on a continuous scale, all dimensional measures (Min_diffabs, Max_diffabs, VSsigned,abs, VSunsigned, A1, A2, RoM; in mm) were normalised to horse size through division by hip height (in m). Dimensionless speed Vhat (Srinivasan and Ruina, 2006) was calculated based on average trotting speed (v) from GPS data, the horses’ hip height (L) and gravitational acceleration (g, 9.81 m s2) as:

v

Vhat ¼ pffiffiffiffiffiffiffiffiffi : gL For each trotting direction (straight, left and right rein), random regression was performed across the mean values for Vhat and all calculated measures of the 10 horses using a linear mixed model in SPSS (PASW Statistics 18). A common slope significantly different from zero would then indicate a systematic effect of Vhat on measures across horses. Results were considered significant at P 6 0.05.

Results

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

Subjective assessment

Range of movement (RoM) was calculated as the difference between maximum and minimum displacement of a stride.

During trot in a straight line, speed had a significant effect on the number of horses declared sound (P = 0.018), with more horses

Fig. 3. Direct comparison between subjective and objective assessment of ten horses trotting at a slow, preferred and fast speed on the straight and circle. Hollow wide bars, subjective lameness score; solid thin bars, objective unsigned vector sum (VSunsigned); checked thin bars, signed vector sum (VSsigned,abs), OS, os sacrum. Green, trot in a straight line; blue, trot in a circle on the left rein; red, trot in a circle on the right rein. Curly brackets indicate significant Friedman test, bold bracket: subjective assessment, thin bracket: objective assessment. Subjective assessment based on the 11-point UK scoring system (Wyn-Jones, 1988; 0 = sound, 10 = non-weight bearing lame), showing the mean ± SEM score across the ten horses as assigned to the forelimbs (left column) and hind limbs (right column). The low lameness scores reflect the population of subtly lame horses. Objective assessment based on VSunsigned and VSsigned,abs for head movement (left column) and sacrum movement (right column), showing the mean ± SEM (VSunsigned) and median ± interquartile range (VSsigned,abs) across the 10 horses.

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Table 1 Free marginal kappa for the derived binary classification as lame (yes/no), forelimb lame (yes/no) and hind limb lame (yes/no) for the nine different trotting conditions. Slow

Preferred

Fast

Mean

Lame? Straight line Circle, left rein Circle, right rein

0.29 0.48 0.17

0.20 0.29 0.24

0.13 0.40 0.29

0.21 0.39 0.23

Forelimb lame? Straight line Circle, left rein Circle, right rein

0.47 0.59 0.17

0.45 0.60 0.19

0.79 0.67 0.43

0.57 0.62 0.26

Hind limb lame? Straight line Circle, left rein Circle, right rein

0.11 0.20 0.09

0.17 0.15 0.12

0.13 0.27 0.11

0.14 0.21 0.11

considered sound at higher speeds (Fig. 2). Accordingly, the average lameness score dropped at higher speeds (Fig. 3) and was significantly different between speed categories for both forelimb (P = 0.013) and hind limb lameness (P = 0.029). During trot in a circle on either rein (Figs. 2 and 3), speed did not significantly affect the number of horses declared sound (P P 0.165) or the average lameness score (P P 0.114). Inter-observer agreement was low across conditions (Table 1), being lowest for the presence of hind limb lameness on both straight and circle (mean values of j = 0.11–0.27) and highest for the presence of forelimb lameness at the ‘fast’ speed on the straight (j = 0.79), where most horses were declared sound (Fig. 2). All participants ranked the fast speed as the most difficult to assess. Half of the participants judged assessment at the preferred speed easiest, the other half considered assessment at preferred and slow speed comparable.

Objective assessment of movement asymmetry Details for each condition are presented in Table 2, details on baseline symmetry on the straight for all individual horses are shown in Table 3. VSunsigned and VSsigned,abs at each speed category remained unaffected for both head (P = 0.670) and sacrum (P = 0.741) on the straight (Fig. 3), except for VSsigned,abs of the head (P = 0.045). On the circle, both VSunsigned and VSsigned,abs were significantly different between speed categories for head and sacrum on either rein (P 6 0.027) except for VSsigned,abs of the head on the right rein (P = 0.067), asymmetry increasing at higher speed (Fig. 3). Random regression (Table 4) revealed that during trot in a straight line the common slope was significantly different from zero for SIup,abs, VSsigned,abs, A2 and RoM of the head (P 6 0.050), Max_diffabs, VSunsigned, A1, and MS of the withers (P 6 0.025) and Min_diffabs, A2, MS and RoM of the sacrum (P 6 0.039). These significantly affected measures showed relatively small and inconsistent changes, some indicating a decrease and some an increase in asymmetry at higher speeds. During trot in a circle, the common slope was significantly different from zero on both reins for SIdown,abs, Min_diffabs, A2 and MS of the head (P 6 0.038), SIdown,abs, Max_diffabs, Min_diffabs, VSunsigned, VSsigned,abs, A1, A2 and MS of the withers (P 6 0.012) and SIup,abs, SIdown,abs, Min_diffabs, VSunsigned, VSsigned,abs, A1, A2, MS and RoM of the sacrum (P 6 0.025). In addition, results were significant on the left rein only for Max_diffabs, VSunsigned, VSsigned,abs and A1 of the head (P 6 0.004), SIup,abs of the withers (P = 0.037) and Max_diffabs of the sacrum (P = 0.049). For all significantly affected asymmetry measures on the circle, asymmetry increased markedly with increasing speed. The common slope for Hip_hike_diffabs was significantly different from zero during trot on a straight line (P = 0.005, Slope (CI): 6.74 (11.23, 2.26)) and in a circle on the left rein (P < 0.001,

Table 2 Mean (SD) for speed, dimensionless speed (Vhat), stride frequency and dimensionless stride frequency (Fhat) on the straight and circle in the three speed categories ‘slow’, ‘preferred’ and ‘fast’. Straight Slow Speed (in m s1) Dimensionless speed, Vhat Stride frequency (in Hz) Dimensionless stride frequency, Fhat

2.80 0.80 1.48 0.53

(0.44) (0.11) (0.08) (0.03)

Circle Preferred

Fast

3.55 1.01 1.62 0.58

4.76 1.36 1.81 0.65

(0.37) (0.09) (0.08) (0.03)

Slow (0.58) (0.12) (0.11) (0.03)

2.56 0.73 1.41 0.51

(0.38) (0.09) (0.06) (0.03)

Preferred

Fast

2.95 0.84 1.51 0.54

3.61 1.03 1.68 0.60

(0.33) (0.08) (0.09) (0.03)

(0.40) (0.10) (0.13) (0.05)

Table 3 Mean values for selected asymmetry measures during trot in a straight line at the ‘preferred’ speed. SIup: symmetry index of the two upwards movement amplitudes; ER: energy ratio and MAS: motion asymmetry, both based on the decomposed signal. Horse

1 2 3 4 5 6 7 8 9 10

Forelimb lameness

Hind limb lameness

SIup head

ER withers

MAS head (in%)

SIup OS

ER OS

MAS OS (in%)

0.54a 0.18a 0.12 0.30a 0.08 0.40a 0.21a 0.28a 0.10 0.27a

0.92a 0.99 0.98 0.96 0.98 0.99 0.99 0.93a 0.99 0.96

43b 26 19 33 14 29 19 31 18 26

0.27a 0.16 0.01 0.17a 0.04 0.16 0.03 0.31a 0.12 0.03

0.89a 0.95 0.97 0.92 0.96 0.90 0.98 0.91 0.98 0.91

23 18 12 21 15 24 12 23 12 21

SIup, upwards symmetry index; ER, energy ratio; MAS, motion asymmetry; OS, os sacrum. a Asymmetry outside the mean and 1 SD of sound horses (Buchner et al., 1996; Audigie et al., 2002). MAS: motion asymmetry (Peham et al., 2000), equivalent to 100-MS in % (motion symmetry, see Section ‘Materials and methods’). b Moderately lame according to Peham et al., 2000 (MAS > 40: moderate lameness).

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Table 4 Common slope (95% confidence interval) from linear mixed model (random regression) of all objective measures over dimensionless speed (Vhat). Max_diffabs, Min_diffabs, VSunsigned, VSsigned,abs, A1, A2 and RoM are normalised to horse size by dividing the measure in mm by hip height in m. SIup,abs

SIdown,abs

Straight line Head 0.21a 0.00 (0.38/0.03) (0.10/ 0.11) Withers 0.03 (0.02/ 0.03 0.08) (0.04/ 0.10) OS 0.04 (0.14/ 0.08 0.06) (0.01/ 0.17)

Max_diffabs

Min_diffabs

VSunsigned

VSsigned,abs

6.33 (13.00/ 0.33) 2.12a (0.30/ 3.95)

5.03 3.21 7.97a (10.10/0.04) (8.13/1.71) (14.54/ 1.39) 0.00 (1.97/ 2.22a (0.62/ 3.00 (6.92/ 1.97) 3.82) 0.92)

0.86 3.30a 1.27 0.70 (1.79/ (3.70/1.97) (5.68/0.92) (1.25/3.79) 3.19)

Circle, left rein Head 0.18 (0.26/ 0.63) Withers 0.21a (0.01/ 0.40) OS 0.89a (0.66/ 1.12)

0.76a (0.41/ 24.71a (8.56/ 1.11) 40.85) 0.54a (0.31/ 21.32a 0.77) (10.81/31.82) 0.62a (0.37/ 9.42a (0.05/ 0.87) 18.78)

Circle, right rein Head 0.15 (0.34/ 0.64)

0.67a (0.33/ 6.15 (17.28/ 22.23a (3.03/ 1.01) 29.58) 41.42)

16.91 (9.07/ 20.78 (5.30/ 42.88) 46.58)

Withers 0.12 (0.04/ 0.27) OS 0.37a (0.05/ 0.70)

0.47a (0.25/ 12.51a (4.49/ 0.69) 20.53) 0.53a (0.34/ 1.51 (5.81/ 0.71) 8.84)

17.20a (8.17/ 16.29a (4.11/ 26.23) 28.46) 18.77a (8.89/ 21.04a (8.87/ 28.66) 33.20)

13.48a (0.81/ 26.14) 11.34a (2.74/ 19.94) 28.08a (16.90/ 39.27)

12.84a (3.50/ 22.17) 20.19a (8.89/ 31.49)

31.09a (16.79/45.38) 23.29a (13.13/33.44) 29.54a (19.99/39.09)

25.71a (9.59/ 41.82) 23.17a (11.69/ 34.64) 27.42a (16.28/ 38.56)

A1

A2

MS

RoM

1.10 3.16a (5.50/ (3.69/1.48) 0.83)

0.56 (6.99/ 5.87)

9.06a (14.56/ 3.56)

1.22a (0.44/ 1.99)

5.73a (8.60/ 2.85)

2.81 (7.36/ 1.75)

2.09 (4.25/ 0.08)

0.76 (0.65/ 7.69a (9.87/ 5.50) 2.18)

9.17a (14.10/ 14.87a 4.24) (19.37/10.37)

17.24a (9.59/ 10.63a (15.60/5.65) 24.89) 12.76a (6.75/ 6.56a (11.23/ 18.77) 1.90) 14.67a (9.76/ 15.62a 19.58) (19.36/11.89)

44.40a (59.57/29.24) 34.79a (49.45/20.13) 55.43a (69.54/41.32)

11.77 (1.34/ 24.89) 9.70a (4.56/ 14.84) 10.44a (6.24/ 14.63)

2.87 (11.07/ 16.80) 5.84 (4.31/ 15.98) 10.99a (21.45/0.32)

14.84a 41.06a 9.91 (29.86/ (18.74/10.94) (66.17/15.95) 10.03) 11.37a (16.33/6.42) 17.02a (21.42/12.62)

33.66a (47.85/19.47) 46.19a (58.83/33.55)

8.23 (20.09/ 3.64) 18.55a (28.41/8.69)

SIup,abs, absolute value for upwards symmetry index; SIdown,abs, absolute value for downward symmetry index; Max_diffabs, absolute value for difference between two maxima; Min_diffabs, absolute value for difference between two minima; VSunsigned, unsigned vector sum; VSsigned,abs, signed vector sum; A1, first harmonic amplitude (asymmetrical component); A2, second harmonic amplitude (symmetrical component); MS, motion symmetry; RoM, range of movement; OS, os sacrum. a Slope significantly different from zero (a = 0.05)

Slope (CI): 34.68 (21.29, 48.08)), but not on the right rein (P = 0.209).

Discussion This study investigated the effect of trotting speed on subjective and objective evaluation of subtle lameness. Changes in trotting speed had different effects on subjective and objective evaluation. During trot in a straight line, increasing speed resulted in more horses being subjectively declared sound with a corresponding decrease in average lameness score; in contrast, objective VSunsigned and VSsigned,abs did not show a significant decrease in asymmetry except for VSsigned,abs of the head. During trot in a circle, changes in speed did not systematically affect subjective assessment; in contrast, objective VSunsigned and VSsigned,abs were significantly different and movement asymmetry increased with increasing speed except for VSsigned,abs of the head on the right rein. These results show that during evaluation in a straight line, it is advisable to trot a horse at a slow speed when uncertain about the presence of lameness; this will help to visually appreciate subtle asymmetry. As scores were found to be unaffected by trotting speed on the circle, lunging can aid consistency during the decision process. We found mostly low inter-observer agreement across trotting conditions (Table 1), matching low agreement reported for horses with mild (score <1.5/5) lameness (Keegan et al., 2010). In accordance with Keegan et al. (2010), agreement on presence of forelimb lameness was higher than for hind limb lameness. However, more horses were considered free of forelimb lameness, which may have contributed to the better agreement. On the straight, the difference between subjective and objective response to increasing speed might be an interaction of several parameters. Random regression revealed that SIup,abs and VSsigned,abs for the head and Min_diffabs for the sacrum showed a slight but significant decrease in asymmetry with increasing speed

when examined on a continuous scale; in contrast, MS for the sacrum showed an increase in asymmetry. Increasing stride frequency and significantly reduced range of motion for head and sacrum may make asymmetry more difficult to see: participants noted that at the fast speed ‘the gait was just too fast’, they ‘could not keep up’ and fast trot ‘just masked the lameness’. These observations might be supported by frequency dependent thresholds when discriminating visual stimuli (Holcombe, 2009), although the complexity of natural scenes like the one in this study would only allow for speculation which exact features limit asymmetry perception. On the circle, while speed did not affect subjective scoring, most investigated objective asymmetry measures showed a significant and pronounced increase in movement asymmetry with increasing speed. The explanation for this discrepancy between perception and measurement may result from a combination of increased movement frequency (reducing the visibility of asymmetry) and increased movement asymmetry (improving the visibility of asymmetry) on the circle; we hypothesise that the two effects offset each other, resulting in the perception of a similar lameness degree across speed categories while objectively differing. Alternatively, veterinarians may assess other parameters on the circle (related to e.g. limb movement and rhythm) that are independent of speed and do not translate into systematic asymmetry changes of head and pelvis. One participant mentioned possibly intuitively adjusting the lameness score to the speed on the circle due to subconscious knowledge about changes in lameness with speed. Further work is needed to better understand these interactions. During trot in a straight line, VSsigned,abs of the head followed the significant decrease in subjective lameness score in contrast to VSunsigned. This may be related to an inconsistent nod-down pattern, also commonly referred to as ‘switching limb lameness’. If a forelimb lame horse was nodding down equally on left and right limb, mean/median VSsigned can be close to zero and the amount of relevant asymmetry may be underestimated. In contrast, VSunsigned reflects the amount of asymmetry regardless of its

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directionality and the amount of relevant asymmetry may be overestimated. The reliability of the UK grading scale has previously been questioned, as ‘the points on the scale have no absolute definition’ (Dyson, 2011). We found mean (SD) score ranges of 0.90 (0.88) to 1.90 (0.57) across observers when assessing the ten horses at the preferred speed, ranges commonly spanning 0/10–2/10. Greatest variance in scores was also qualitatively found around the lower grade AAEP scores by Keegan et al. (2010). Exact lameness scores should therefore be regarded with caution, especially when following treatment between different institutions or assessors and also in light of within-observer variation in the assigned score on repeated occasions (Keegan et al., 1998; Arkell et al., 2006; Fuller et al., 2006). Objective measurements for trot in a straight line compared well with the literature. The mean ‘preferred’ trotting speed of 3.6 m/s matched previously published speeds of 3.96 m/s (Galisteo et al., 1998) and 3.88 m/s (Holmström et al., 1995) in taller horses (average withers height 1.58 and 1.54 m, respectively, compared to our 1.41 m). The average speed margins of 2.8–4.8 m/s were slightly less wide than reported for treadmill locomotion (1.81– 4.78 m/s for a 170 kg pony and 1.42–5.46 m/s for a 680 kg horse; Heglund and Taylor, 1988), possibly due to differences in training and limits in the running capacity of the handler. Increasing speed caused a significant decrease in range of movement for head and sacrum but not for the withers, matching previous studies into head movement (Peham et al., 2000; Robert et al., 2002) and withers/sacrum movement (Robert et al., 2001). We found no evidence for systematic exacerbation of subtle lameness with increasing trotting speed, in line with Peham et al. (2000). Objective measurements for trot in a circle compared well with the available literature. The mean ‘preferred’ speed of 3.0 m/s was the same as in dressage horses on an average 4.6 m radius circle on a soft surface (Pfau et al., 2012), slower than approximately 3.7 m/s found in horses on a 5.0 m radius circle on a soft surface (Hobbs et al., 2011) and faster than 2.3 m/s found in horses on a 3.0 m radius circle on a hard/rubberised surface (Clayton and Sha, 2006), most likely due to differences in horse size, surfaces and radius. A circle-related asymmetry bias as observed in this study has previously been found for the centre of mass movement of the head/ neck segment and whole body (Clayton and Sha, 2006) and several upper-body landmarks of sound horses (Starke et al., 2012a). In agreement with findings for sound horses trotting on a soft circle (Pfau et al., 2012), we found no systematic effect of speed on SIup,abs for the head and a systematic effect on Min_diffabs and Max_diffabs for head and sacrum, although Max_diffabs only showed a significant common slope on the left rein in the present study. This finding supports previous observations that horses may adapt differently to movement on the left and right rein (Starke et al., 2012a; Pfau et al., 2012). Differences in movement on left and right rein may, for example, be related to learned or genetically determined ‘laterality’, ‘lateralised motor behaviour’, ‘handedness’ or ‘sidedness’ (Drevemo et al., 1987; Murphy et al., 2005; Van Dierendonck et al., 2005; McGreevy and Thomson, 2006; Williams and Norris, 2007), perceptual preferences and visual left side bias (De Boyer Des Roches et al., 2008; Austin and Rogers, 2012) or adaptive morphological changes between left and right limbs in relation to performance (Watson et al., 2003; Pearce et al., 2005). All our horses were mares and always handled from the left, but unridden/untrained and not bred for a specific discipline which could have introduced a selective bias in gene pool. The small sample size however does not allow for any further conclusions concerning adaptations on left and right rein. Since the response to changes in speed appears to depend on the baseline lameness severity at least on the straight, results from the study presented here should not be extrapolated to the general

horse population seen in the equine clinic: Horses with more prominent lameness are likely to increase asymmetry at higher speeds (Peham et al., 2000; Chateau et al., 2007). This differential response in asymmetry modification may be related to changes in limb loading at higher speeds: (Robert et al., 2002) measured increased flexion of fore- (increased fetlock hyperextension and shoulder flexion) and hind limbs (increased flexion of hip, stifle and tarsal joints) during impact and support phase with increasing speed and associated this with increased limb loading. In overground studies peak vertical forces increased with trotting speed only in the forelimbs (McLaughlin et al., 1996; Dutto et al., 2004), although on the treadmill increasing in both fore and hind limbs (Weishaupt et al., 2010). Despite conflicting evidence for speed dependency of braking and propulsive forces in fore and hind limbs (McLaughlin et al., 1996; Dutto et al., 2004), forelimb lameness might be amplified differently by speed changes than hind limb lameness during trot on the straight; more work is needed to better understand these dependencies. Conclusions During visual assessment of subtle lameness on the straight, a slow trotting speed can enhance the visual detection of subtle asymmetry and should therefore be added to the gait examination in cases of uncertainty. Assessment on the circle did not suffer from this speed-related bias. While during trot in a straight line speed effects are likely to depend on the grade of baseline lameness, during trot in a circle changes in speed should always be assumed to systematically affect objective lameness quantification, measurable asymmetry increasing at higher speeds for sound and subtly lame horses. Speed should therefore always be controlled (or at least measured) during repeated assessment to exclude the interaction between speed effects, baseline lameness and effects of clinical intervention. This is especially important when interpreting results from objective gait analysis. In future, it would be valuable to investigate methods for objective lameness quantification on the circle that are robust against changes in lunging condition. 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 We would like to thank William H. Barker, David Bolt, Anna C. Dalton, Andrew Fiske-Jackson and Thomas H. Witte for their valued time and expertise in assessing the horses, Jim Usherwood for helpful comments on normalising speed and two anonymous reviewers for their constructive comments on the manuscript. S.D. Starke is funded through a PhD studentship by the Royal Veterinary College. 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. Veterinary Record 159, 346–348. Audigie, 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. Austin, N.P., Rogers, L.J., 2012. Limb preferences and lateralization of aggression, reactivity and vigilance in feral horses, Equus caballus. Animal Behaviour 83, 239–247. Barr, A.R., Dow, S.M., Goodship, A.E., 1995. Parameters of forelimb ground reaction force in 48 normal ponies. Veterinary Record 136, 283–286.

S.D. Starke et al. / The Veterinary Journal 197 (2013) 245–252 Baxter, G.M., Stashak, T.S., 2011. Examination for lameness. In: Baxter, G.M. (Ed.), Adams and Stashak’s Lameness in Horses. Wiley-Blackwell, West Sussex, UK, pp. 115; 143–149; 151–153. Blue Cross, 2011. New Survey Reveals UK’s Current Equine Healthcare Problems. www.bluecross.org.uk/2000-84227/new-survey-reveals-uks-current-equinehealthcare-problems-.html (accessed 30 October 2012). Brennan, R.L., Prediger, D.J., 1981. Coefficient kappa – Some uses, misuses, and alternatives. Educational and Psychological Measurement 41, 687–699. 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. Busschers, E., Van Weeren, P.R., 2001. Use of the flexion test of the distal forelimb in the sound horse: Repeatability and effect of age, gender, weight, height and fetlock joint range of motion. Journal of Veterinary Medicine Series A 48, 413– 427. Chateau, H., Renard, L., Falala, S., Valette, J.-P., Audigié, F., Pourcelot, P., Ravary, B., Pacquet, L., Denoix, J.-M., Crevier-Denoix, N., 2007. A method for quantifying vertical displacements of the trunk and gait symmetry in horses trotting at high speed. Computer Methods in Biomechanics and Biomedical Engineering 10, 165–166. Clayton, H.M., 1994. Comparison of the stride kinematics of the collected, working, medium and extended trot in horses. Equine Veterinary Journal 26, 230–234. 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., 462–467. De Boyer Des Roches, A., Richard-Yris, M.-A., Henry, S., Ezzaouïa, M., Hausberger, M., 2008. Laterality and emotions: Visual laterality in the domestic horse (Equus caballus) differs with objects’ emotional value. Physiology and Behavior 94, 487–490. Degueurce, C., Pourcelot, P., Audigie, F., Denoix, J.M., Geiger, D., 1997. Variability of the limb joint patterns of sound horses at trot. Equine Veterinary Journal Suppl., 89–92. Drevemo, S., Fredricson, I., Hjerten, G., Mcmiken, D., 1987. Early development of gait asymmetries in trotting Standardbred colts. Equine Veterinary Journal 19, 189– 191. Dutto, D.J., Hoyt, D.F., Cogger, E.A., Wickler, S.J., 2004. Ground reaction forces in horses trotting up an incline and on the level over a range of speeds. Journal of Experimental Biology 207, 3507–3514. Dyson, S., 2011. Can lameness be graded reliably? Equine Veterinary Journal 43, 379–382. 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. Fuller, C.J., Bladon, B.M., Driver, A.J., Barr, A.R.S., 2006. The intra- and inter-assessor reliability of measurement of functional outcome by lameness scoring in horses. The Veterinary Journal 171, 281–286. Galisteo, A.M., Cano, M.R., Morales, J.L., Vivo, J., Miro, F., 1998. The influence of speed and height at the withers on the kinematics of sound horses at the hand-led trot. Veterinary Research Communications 22, 415–423. Halling Thomsen, M., Tolver Jensen, A., Sorensen, H., Lindegaard, C., Haubro Andersen, P., 2010. Symmetry indices based on accelerometric data in trotting horses. Journal of Biomechanics 43, 2608–2612. Heglund, N.C., Taylor, C.R., 1988. Speed, stride frequency and energy-cost per stride – How do they change with body size and gait. Journal of Experimental Biology 138, 301–318. Hobbs, S.J., Licka, T., Polman, R., 2011. The difference in kinematics of horses walking, trotting and cantering on a flat and banked 10 m circle. Equine Veterinary Journal 43, 686–694. Holcombe, A.O., 2009. Seeing slow and seeing fast: Two limits on perception. Trends in Cognitive Sciences 13, 216–221. Holmström, M., Fredricson, I., Drevemo, S., 1995. Biokinematic effects of collection on the trotting gaits in the elite dressage horse. Equine Veterinary Journal 27, 281–287. Jeffcott, L.B., Rossdale, P.D., Freestone, J., Frank, C.J., Towers-Clark, P.F., 1982. An assessment of wastage in Thoroughbred racing from conception to 4 years of age. Equine Veterinary Journal 14, 185–198. Kaneene, J.B., Ross, W.A., Miller, R., 1997. The Michigan equine monitoring system. II. Frequencies and impact of selected health problems. Preventive Veterinary Medicine 29, 277–292. Keegan, K.G., 2007. Evidence-based lameness detection and quantification. Veterinary Clinics of North America: Equine Practice 23, 403–423. Keegan, K.G., Wilson, D.A., Wilson, D.J., Smith, B., Gaughan, E.M., Pleasant, R.S., Lillich, J.D., Kramer, J., Howard, R.D., Bacon-Miller, C., et al., 1998. Evaluation of mild lameness in horses trotting on a treadmill by clinicians and interns or residents and correlation of their assessments with kinematic gait analysis. American Journal of Veterinary Research 59, 1370–1377. Keegan, K.G., Dent, E.V., Wilson, D.A., Janicek, J., Kramer, J., Lacarrubba, A., Walsh, D.M., Cassells, M.W., Esther, T.M., Schiltz, P., et al., 2010. Repeatability of subjective evaluation of lameness in horses. Equine Veterinary Journal 42, 92– 97. Keegan, K.G., Macallister, C.G., Wilson, D.A., Gedon, C.A., Kramer, J., Yonezawa, Y., Maki, H., Pai, P.F., 2012. Comparison of an inertial sensor system with a

251

stationary force plate for evaluation of horses with bilateral forelimb lameness. American Journal of Veterinary Research 73, 368–374. Kramer, J., Keegan, K.G., Kelmer, G., Wilson, D.A., 2004. Objective determination of pelvic movement during hind limb lameness by use of a signal decomposition method and pelvic height differences. American Journal of Veterinary Research 65, 741–747. Leach, D.H., Drevemo, S., 1991. Velocity-dependent changes in stride frequency and length of trotters on a treadmill. In: Equine Exercise Physiology, vol. 3. ICEEP Publications, Davis, California, pp. 136–140. Leach, K.A., Tisdall, D.A., Bell, N.J., Main, D.C.J., Green, L.E., 2012. The effects of early treatment for hindlimb lameness in dairy cows on four commercial UK farms. The Veterinary Journal 193, 626–632. Licka, T., Kapaun, M., Peham, C., 2004. Influence of rider on lameness in trotting horses. Equine Veterinary Journal 36, 734–736. May, S.A., Wyn-Jones, G., 1987. Identification of hindleg lameness. Equine Veterinary Journal 19, 185–188. McCracken, M.J., Kramer, J., Keegan, K.G., Lopes, M., Wilson, D.A., Reed, S.K., Lacarrubba, A., Rasch, M., 2012. Comparison of an inertial sensor system of lameness quantification with subjective lameness evaluation. Equine Veterinary Journal. http://dx.doi.org/10.1111/j.2042-3306.2012.00571.x (ePub ahead of print). McGreevy, P.D., Thomson, P.C., 2006. Differences in motor laterality between breeds of performance horse. Applied Animal Behaviour Science 99, 183–190. McLaughlin Jr., R.M., Gaughan, E.M., Roush, J.K., Skaggs, C.L., 1996. Effects of subject velocity on ground reaction force measurements and stance times in clinically normal horses at the walk and trot. American Journal of Veterinary Research 57, 7–11. Murphy, J., Sutherland, A., Arkins, S., 2005. Idiosyncratic motor laterality in the horse. Applied Animal Behaviour Science 91, 297–310. Parkes, R.S.V., Weller, R., Groth, A.M., May, S., Pfau, T., 2009. Evidence of the development of ‘domain-restricted’ expertise in the recognition of asymmetric motion characteristics of hindlimb lameness in the horse. Equine Veterinary Journal 41, 112–117. Pearce, G.P., May-Davis, S., Greaves, D., 2005. Femoral asymmetry in the Thoroughbred racehorse. Australian Veterinary Journal 83, 367–370. Peham, C., Scheidl, M., Licka, T., 1996. A method of signal processing in motion analysis of the trotting horse. Journal of Biomechanics 29, 1111–1114. Peham, C., Licka, T., Mayr, A., Scheidl, M., Girtler, D., 1998. Speed dependency of motion pattern consistency. Journal of Biomechanics 31, 769–772. Peham, C., Licka, T., Mayr, A., Scheidl, M., 2000. Individual speed dependency of forelimb lameness in trotting horses. The Veterinary Journal 160, 135–138. Pfau, T., Witte, T.H., Wilson, A.M., 2005. A method for deriving displacement data during cyclical movement using an inertial sensor. Journal of Experimental Biology 208, 2503–2514. Pfau, T., Stubbs, N., Kaiser, L., Brown, L., Clayton, H.M., 2012. The effect of trotting speed and circle radius on movement symmetry in horses during lunging on a soft surface. American Journal of Veterinary Research 73, 1890–1899. Ramey, D.W., 1997. Prospective evaluation of forelimb flexion tests in practice: Clinical response, radiographic correlations, and predictive value for future lameness. In: Proceedings of the Annual Convention of the AAEP 1997, pp. 116– 120. Randolph, J.J., 2005. Free-marginal multirater kappa: An alternative to Fleiss’ fixedmarginal multirater kappa. Presented at Joensuu Learning and Instruction Symposium, Joensuu, Finland. Robert, C., Audigié, F., Valette, J.P., Pourcelot, P., Denoix, J.M., 2001. Effects of treadmill speed on the mechanics of the back in the trotting saddlehorse. Equine Veterinary Journal 33, 154–159. Robert, C., Valette, J.P., Pourcelot, P., Audigié, F., Denoix, J.M., 2002. Effects of trotting speed on muscle activity and kinematics in saddlehorses. Equine Veterinary Journal 34, 295–301. Ross, M.W., 2011a. Movement. In: Ross, M.W., Dyson, S.J. (Eds.), Diagnosis and Management of Lameness in the Horse. Elsevier Saunders, Missouri, USA, pp. 66; 77–78. Ross, M.W., 2011b. Manipulation. In: Ross, M.W., Dyson, S.J. (Eds.), Diagnosis and Management of Lameness in the Horse. Elsevier Saunders, Missouri, USA, pp. 80–88. Ross, W.A., Kaneene, J.B., Caron, J.P., Gallagher, K.F., Gardiner, J.C., 1999. Factors influencing recovery from and duration of lameness in Michigan (USA) horses. Preventive Veterinary Medicine 40, 127–138. Srinivasan, M., Ruina, A., 2006. Computer optimization of a minimal biped model discovers walking and running. Nature 439, 72–75. Starke, S.D., Willems, E., May, S.A., Pfau, T., 2012a. Vertical head and trunk movement adaptations of sound horses trotting in a circle on a hard surface. The Veterinary Journal 193, 73–80. Starke, S.D., Witte, T.H., May, S.A., Pfau, T., 2012b. Accuracy and precision of hind limb foot contact timings of horses determined using a pelvis-mounted inertial measurement unit. Journal of Biomechanics 45, 1522–1528. Starke, S.D., Willems, E., Head, M., May, S.A., Pfau, T., 2012c. Proximal hind limb flexion in the horse: effect on movement symmetry and implications for defining soundness. Equine Veterinary Journal 44, 657–663. Uhlir, C., Licka, T., Kubber, P., Peham, C., Scheidl, M., Girtler, D., 1997. Compensatory movements of horses with a stance phase lameness. Equine Veterinary Journal Supplement 23, 102–105. Van Dierendonck, M.C., van Heel, M.C.V., Kroekenstoel, A.M., Back, W., 2005. Development of grazing posture preference in foals (0–1 Yr) and their dams and

252

S.D. Starke et al. / The Veterinary Journal 197 (2013) 245–252

its relation to other asymmetrical behaviours. In: Current Issues and Research in Veterinary Behavioral Medicine: Papers Presented at the 5th International Veterinary Behavior Meeting, 2005. Purdue University Press, pp. 85–87. Van Weeren, P.R., Van Den Bogert, A.J., Back, W., Bruin, G., Barneveld, A., 1993. Kinematics of the Standardbred trotter measured at 6, 7, 8 and 9 m/s on a treadmill, before and after 5 months of prerace training. Acta Anatomica 146, 154–161. Verschooten, F., Verbeeck, J., 1997. Flexion test of the metacarpophalangeal and interphalangeal joints and flexion angle of the metacarpophalangeal joint in sound horses. Equine Veterinary Journal 29, 50–54. Vigre, H., Chriél, M., Hesselholt, M., Falk-Rønne, J., Kjær Ersbøll, A., 2002. Risk factors for the hazard of lameness in Danish Standardbred trotters. Preventive Veterinary Medicine 56, 105–117. Warrens, M., 2010. Inequalities between multi-rater kappas. Advances in Data Analysis and Classification 4, 271–286.

Watson, K.M., Stitson, D.J., Davies, H.M., 2003. Third metacarpal bone length and skeletal asymmetry in the Thoroughbred racehorse. Equine Veterinary Journal 35, 712–714. Weishaupt, M.A., Hogg, H.P., Auer, J.A., Wiestner, T., 2010. Velocity-dependent changes of time, force and spatial parameters in Warmblood horses walking and trotting on a treadmill. Equine Veterinary Journal 42, 530–537. Williams, D.E., Norris, B.J., 2007. Laterality in stride pattern preferences in racehorses. Animal Behaviour 74, 941–950. Wren, T.A.L., Rethlefsen, S.A., Healy, B.S., Do, K.P., Dennis, S.W., Kay, R.M., 2005. Reliability and validity of visual assessments of gait using a modified physician rating scale for crouch and foot contact. Journal of Pediatric Orthopaedics 25, 646–650. Wyn-Jones, G., 1988. Equine Lameness. Blackwell Scientific Publications, Oxford, UK, pp. 3; 5–6; 6–8.