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PLOS One logoLink to PLOS One
. 2024 Jul 30;19(7):e0308061. doi: 10.1371/journal.pone.0308061

Prevalence of movement asymmetries in high-performing riding horses perceived as free from lameness and riders’ perception of horse sidedness

Ebba Zetterberg 1,*, Emma Persson-Sjodin 1, Johan Lundblad 1, Elin Hernlund 1, Marie Rhodin 1
Editor: Rebecca Lee Smith2
PMCID: PMC11288442  PMID: 39078818

Abstract

A high proportion of horses in training, perceived as free from lameness by their owner, exhibit vertical movement asymmetries. These types of asymmetries are sensitive measures of lameness, but their specificity as indicators of orthopaedic pathology or locomotor function remains unclear. Equine athletes performing at a high level could be assumed to exhibit a higher degree of movement symmetry compared with the general horse population, but this has not been confirmed. This study investigated the prevalence of movement asymmetries in horses performing at a high level in three equestrian disciplines; show jumping, dressage and eventing, as well as the association between riders’ perception of horse sidedness and said movement asymmetries. Using an inertial measurement unit-based system (Equinosis), gait analysis was performed on 123 high-performing horses. The mean difference between the two vertical minimum and between the two maximum values of each stride was recorded for the head (HDmin, HDmax) and pelvis (PDmin, PDmax). The horses were defined as asymmetric if one or multiple asymmetry parameters exceeded an absolute trial mean of: >6mm for HDmin or HDmax, and >3mm for PDmin or PDmax, with standard deviation less than the respective mean value. Based on the results, 70% of the horses were classified as asymmetric, which is similar to previous findings for young riding horses and horses competing at a lower level. More than one-third of these high-performing horses had asymmetry values of similar magnitude to those seen in clinically lame horses. No clear associations were observed between rider-perceived sidedness and the vertical movement asymmetry values, indicating that the perceived unevenness between sides is not a determinant of vertical movement asymmetry. Longitudinal studies on movement asymmetries in relation to training intensity and full clinical examinations with local or systemic analgesic testing are desired as further research to determine whether these movement asymmetries indicate a welfare problem.

Introduction

Orthopaedic disorders are a common health problem among horses [1] and a common cause of early retirement from an athletic career [1, 2], impairing the welfare of the horse and with substantial economic and emotional consequences for the owner. Visual detection of lameness by veterinarians and trainers is known to be difficult, especially as regards low-degree lameness [35]. Orthopaedic issues thus run the risk of remaining undetected and progressing into severe or chronic problems before becoming apparent. Objective gait analysis can improve lameness evaluation, as it is less biased and more accurate in quantifying vertical movement asymmetries of the head, withers and pelvis [69]. However, the specificity of measured asymmetry parameters is a highly debated topic [10, 11]. Several studies on populations of horses perceived as free from lameness by their owners have found high prevalences of vertical movement asymmetries [1216], many of the same magnitude as in clinically lame horses [17, 18]. These studies did not investigate the association of movement asymmetries with painful pathologies, but highlight the potential welfare problem should this be the case. As visual detection of lameness is difficult [35] and subjective evaluation by a veterinarian may differ from the owner’s assumption of soundness [19], it is difficult to definitively exclude pathology and thereby lameness as a cause of movement asymmetries in these populations of horses. Non-painful factors, e.g. biological variations such as conformational variations or mechanical restrictions, have been discussed as potential sources for these movement asymmetries [12, 14, 20]. This is supported by reports of relatively high prevalence of movement asymmetries among young foals [21] and young trotters even before initiation of training [20]. Laterality is another potential cause of movement asymmetries. Defined as “bias behaviour” or the preference to use one side of the body [2224], laterality could in theory alter the symmetry of movement between the horse’s right and left side. The concept of a horse having a strong and a weak side is well-known among riders, as summarised by Byström et al. [24]. Riders’ perceived sidedness of the horse can be quantified and investigated for its association with movement asymmetries. It has been done for a group of young horses perceived as non-lame by the owners [25]. No association between rider-perceived sidedness and vertical movement asymmetries was seen in that study, despite the horses having a high prevalence of movement asymmetries [25]. However, sidedness may also be affected by age, as size and anatomical proportions change over time [26], and by training [27]. Horses at higher competition levels can be assumed to exhibit less sidedness, given that riders strive to develop equal strength and suppleness in each direction so that the horse can perform the advanced movements required in dressage or the sharp turns required in show jumping. Additionally, riders competing at higher levels may be more skilled in assessing the sidedness of their horses compared with riders in the previous study on young horses [25]. The rider’s perceived sidedness and its relation to movement symmetry may therefore differ between high-performing horses and youngsters.

Horses need to perform well to compete at the highest level. With lameness described as a performance-limiting factor [28], high-performing horses might be thought to exhibit a lower prevalence of lameness compared to the general equine population. Additionally, these horses undergo regular scrutiny by veterinarians (e.g. at horse inspections) while participating in high-level competitions and are frequently observed by trainers and judges, thus potentially increasing the probability of detecting lameness. However, our knowledge about the prevalence of movement asymmetries among horses competing at a higher level is limited. Therefore, the aim of this study was to investigate the prevalence of vertical movement asymmetries among high-performing horses in three different disciplines; show jumping, dressage and eventing. Riders’ perceptions of sidedness in the horses and the association with objectively quantified movement asymmetries were also investigated.

Material and methods

Horses

A convenience sample of high-performing show jumpers, dressage and eventing horses was recruited for the study through social media advertisements and personal contacts between 2016 and 2023. Horses had to be perceived as non-lame by the owner, at the time of gait analysis and had to have no reported treatment for orthopaedic disease within the previous three months. They also had to have participated in competitions at the required level within the previous six months. For each discipline, the required level of competition for inclusion was: (i) 140 cm for jumping, (ii) Prix St George (or Swedish equivalent) for dressage and (iii) three-star competition (CCI3*/CIC3*) for eventing (note classification change made 2019, lower requirements after 2019 for CCI3*). Riders (not necessarily the same person as the owner) were asked to fill out a questionnaire about the horse and its history of lameness. All owners/riders provided written informed consent for participation in the study. In accordance with Swedish legislation (SJVFS 2019:9), no ethical permission was needed as the animals were privately owned and no invasive procedures were carried out.

Objective gait analysis

An inertial measurement units (IMU) based gait analysis system (Equinosis Q with Lameness Locator, St. Louise, MO, USA), was used. Each horse was fitted with three IMUs, in the following three anatomical locations; the poll, attached using a custom-made head bumper; the dorsal surface of the right pastern, attached using a pastern wrap; and the pelvis, attached using double-sided adhesive tape on the midline between the tubera sacrale. Gait analysis was performed in trot in four different conditions: straight line on a hard surface (concrete or packed dirt road) and straight line and lungeing, in both directions aiming for a circle with a 10-meter diameter, on a soft arena surface (sand or sand-fibre). The aim was to collect at least 20 strides for straight-line trials and 25 strides in each lungeing direction. During gait analysis, the trials were recorded using a hand-held video camera. The horses were handled by the riders/caretakers in their home environment.

Data processing

Data from the gait analysis trials were obtained with the Equinosis software, which generated vertical displacement data for the head and the pelvis. For each stride, the differences between the two minimum and the two maximum vertical positions of the head and of the pelvis were calculated. The stride-by-stride data were exported to Matlab (Release 2021b, MathWorks Inc.). Outlier removal for the head parameters was performed automatically as standard, with each stride value compared to the average value of all strides using the Mahalanobis distance method. Stride parameter values exceeding the mean (for the respective parameter) by three or more standard deviations were removed. This procedure was repeated iteratively until no more outliers were found. Video recordings from the trials were also scrutinised. For horses with excessive inconsistent head movements, e.g. biting at handler or head shaking in small sections of the trials, the sequences of strides where this occurred were removed manually before data processing. For each horse and trial, mean values and standard deviation (SD) were determined for each of the four asymmetry parameters, i.e. head maximum position difference (HDmax), head minimum position difference (HDmin), pelvis maximum position difference (PDmax) and pelvis minimum position difference (PDmin). Number of strides and mean stride duration in each trial were also determined. Positive values of the asymmetry parameters indicated movement asymmetries associated with the right fore or hind limb and negative values indicated movement asymmetries associated with the left fore or hind limb. Trials with too few strides, after data processing and outlier removal, were excluded, i.e. lunge trials with less than 25 strides and straight-line trials with less than 20 strides (unless SD was less than the mean value for all asymmetry parameters, in which case straight-line trials with 16–20 strides were accepted).

Sidedness questionnaire

Through convenience sampling, a sub-set of the riders was selected and asked to fill out a questionnaire about perceived sidedness of the horse, either at the same time as the gait analysis or in retrospect. The questionnaire comprised 22 questions regarding perceived differences between the left and right side of the horse during specific dressage movements and when jumping, as well as questions about lateralised behaviour of the rider (S1 Text). The questionnaire was based on conventionally used descriptions of a horse with a believed weaker and stronger side and on rider experiences that can be hypothesised to arise from lateralised behaviour in the horse. To reduce the risk of type 1 errors, closely related questions, identified based on the content of the question and with the use of contingency tables (plotting responses and subjectively assessing for clear relationship in the form of overlapping), were reduced to one representative question. The question with the most answers (fewest non-answers, “na”) was picked to represent that group of questions. Questions in which over 50% of responders did not perceive sidedness were excluded from the analysis. In total, five questions (Table 1) were used for statistical analysis of the association with vertical movement asymmetries.

Table 1. The five questions on rider-perceived sidedness and the respective asymmetry parameter/s used for statistical analysis of the association between rider-perceived sidedness and objectively measured vertical movement asymmetry of the head and pelvis.

Question Pre-set answer options Fixed factor Response variable
1. Do you perceive your horse as exhibiting a sidedness? No/mild/moderate/severe No/mild/ moderate TASstraight/TASlunge
2. Do you perceive your horse as having a weaker hind limb? No/left/right No/Yes PDmin/PDmax
3. Do you perceive your horse as leaning more on either of the reins? No/left/right No/Yes HDmin/HDmax
4. Do you perceive your horse as drifting out on the circle? No/left circle/right circle No/Yes HDmin/HDmax/PDmin/PDmax
5. Do you perceive yourself as having unequal sides with one side perceived as more difficult to ride in? No/left/right No/Yes HDmin/HDmax/PDmin/PDmax

Questions selected based on the researchers’ hypotheses regarding possible association with measured movement asymmetry. Pre-set answers and response variable delimited by /. Answers used as graded sidedness or as binary answers. The response variable tested against each question is shown in the right column. Abbreviations: HDmin/max, mean difference in head minimum/maximum positions between right and left portions of the strides; PDmin/max, mean difference in pelvic minimum/maximum position between right and left portions of the strides; TASstraight/lunge, total movement asymmetry scores in straight-line trials or lungeing trials.

Statistical methods

Descriptive statistics were used to describe asymmetry parameters on group level for all conditions measured. Straight-line trials were used for classification of horses either as symmetric or asymmetric. To quantify the prevalence of movement asymmetries, horses were classified as asymmetric if one or multiple asymmetry parameters exceeded thresholds of mean absolute value >6 mm for HDmax and HDmin, and >3 mm for PDmin and PDmax, with the condition that the SD was less than the respective parameter mean value. The remaining horses were classified as symmetric. These thresholds were based on recommendations by the manufacturer (Equinosis) and reflect the threshold values used clinically. In addition, the prevalence of horses with asymmetry parameters exceeding double the value of the set thresholds (mean absolute value >12 mm for HDmax/min and >6 mm for PDmax/min) was calculated for straight-line trials.

A total asymmetry score, TAS=|HDmin|2+|HDmax|2+|PDmin|+PDmax, for each trial was calculated for the hard surface trial (TASstraight) and a combined score for the lunge trials (TASlunge). The latter was calculated by first adding asymmetry parameter values from both the right and the left lunge trials and then using the sum of each parameter (Sum HDmin/HDmax/PDmin/PDmax) in the TAS equation above.

To identify an association between questionnaire responses and values for the asymmetry parameters, linear mixed-effect models were created in R software (version 4.1.2) [29]. The selected rider-perceived sidedness questions (Table 1) were converted to binary answers; answers of “left” and “right” were converted to “yes”, thus ignoring direction. Asymmetry parameters from straight-line trials on a hard surface and lungeing trials were converted to absolute values, thus indicating a magnitude of asymmetry but not differentiating between sides. This was done to evaluate the association between rider-perceived sidedness and movement asymmetry values, while ignoring whether the direction of the rider-perceived sidedness matched the asymmetry direction. Models were fitted for each questionnaire question and for each asymmetry parameter using the package “lmer” [30]. The response variables were the absolute values of the asymmetry parameters, while the questionnaire answers (binary) were included as fixed factors separately in each model for each asymmetry parameter. Question 1 was modelled against TAS both in straight line and on the lunge. Only two horses were perceived as exhibiting “severe sidedness” and these horses were categorised as displaying “moderate sidedness” in the statistics. Question 2 was modelled against asymmetry parameters of the pelvis in straight-line trials, question 3 was modelled after asymmetry parameters of the head in straight-line trials, and questions 4 and 5 were modelled against asymmetry parameters of both head and pelvis in straight-line trials. Each question and the selected variable testing the association are shown in Table 1. In all models, mean stride duration, as a proxy for speed, was set as a fixed factor and rider was set as a random variable. Assumptions of homoscedasticity and normal distribution were checked using quantile-quantile plots (QQ plots) and residual plots. If the data were considered to be skewed, the Box-Cox method was used to find a transformation closer to normality. Type III ANOVA was performed. Pairwise comparison of the rider-perceived sidedness groups was performed using the package “emmeans” [31]. Significance was set to p < 0.05 for all analyses.

Results

Study population

A total of 125 horses were recruited, but two horses were excluded since they were unable to show steady-state trot without interfering sequences of bucking, tossing of the head etc. Of the remaining 123 horses, 47 were dressage horses, 61 were show jumping horses and 15 were eventing horses. There were 70 geldings, 44 mares and nine stallions, with an age distribution of 6–17 years (median 11 years). The horses belonged to 75 different owners (range 1–5 horses/owner) and there were 122 Warmblood type horses and one Thoroughbred horse. The order of the trials varied among horses. Exclusions due to too few strides were as follows: lunge trials, two horses; straight-line soft surface trials, one horse; straight-line hard surface trials, three horses. Due to lack of access to a hard surface, six horses were only measured on a soft surface. For 11 horses, no straight-line trials on a soft surface were obtained due to missing data. Two horses had sequences of strides manually removed in order to get good sequences of steady-state trot. The sidedness questionnaire was answered for 71 of the horses, by 51 riders, with 80% of the responses retrieved at the time of the gait analysis, 12% within a year and 8% within 14 months after the gait analysis. No difference in results were seen when excluding horses with questionnaire responses not acquired at the time of gait analysis, see S2 Text. Horses with questionnaire responses consisted of 30 show jumpers, 26 dressage horses and 15 eventing horses.

Movement asymmetries in straight-line trot on a hard surface

For straight-line trot on a hard surface, trials by 114 horses were analysed. The mean number of strides per trial was 33 ± 9.7, with a range of 17–63. Three horses had trials with less than 20 strides. Of the 114 horses, 79 (69%) were classified as asymmetric, since they had values of one or multiple asymmetry parameters above the threshold and SD less than its mean. Divided by discipline, asymmetry prevalence was: show jumping 72% (38 of 53), dressage 67% (31 of 46) and eventing 67% (10 of 15). Of the 79 horses classified as asymmetric, 42 (36.8% of the total of 114 horses) had one or multiple asymmetry values above double the set threshold value (double threshold value: >|12| mm for head parameters and >|6| mm for pelvic parameters). Of the 114 horses, 10 horses had high inter-stride variability with one or multiple asymmetry parameters above the threshold, but with a high SD (110–275% of the mean), and were therefore classified as symmetric.

Movement asymmetries in straight-line trot on a soft surface

For straight-line trot on a soft surface, 111 horses were included in the analysis. Mean number of strides per trial was 31 ± 9.8 (range 16–60) and eight horses had trials where the number of strides was below 20. Of the 111 horses, 78 (70%) were classified as asymmetric. Divided by discipline, asymmetry prevalence was: show jumping 66% (37 of 56), dressage 74% (32 of 43) and eventing 75% (9 of 12). Of the 78 horses classified as asymmetric, 33 (29.7% of 111) had one or multiple asymmetry values above double the set threshold values (double threshold values: >|12| mm for head parameters and >|6| mm for pelvic parameters). Of the 111 horses, nine had high inter-stride variability with one or multiple asymmetry parameters above the threshold, but with SD higher than the mean (range 104–189%), and were therefore classified as symmetric.

Comparison of straight-line trials on hard and soft surfaces

Of the 123 horses, 103 had straight-line trials on both hard and soft surfaces. Of the 103 horses, 60 (58.3%) were classified as asymmetric on both hard and soft surfaces, 17 (16.5%) were classified as symmetric on both hard and soft surfaces and 26 (25.2%) were classified as asymmetric on either soft or hard surface, with equal frequency. Table 2 shows mean values of movement asymmetry values for all horses that exceeded thresholds and had SD less than the mean, for both hard and soft surfaces. Right and left orientations of all asymmetry parameters were of equal distribution. There were overall more movement asymmetries associated with mean differences of the minimum position of both pelvis and head (PDmin and HDmin) than with mean differences of the maximum positions (HDmax and PDmax). For the 25% of trials with the highest values (75th percentile), the values for each asymmetry parameter were around double the threshold values or more.

Table 2. Asymmetry parameters exceeding the threshold values (standard deviation (SD) less than mean) presented for horses (n) in straight-line trials on hard and soft surfaces.

Variable n Mean (mm) SD (mm) n above the 75th percentile Mean 75th percentile (mm) Range 75th percentile (mm)
Straight-line hard surface
|HDmin| 39 12.4 4.5 10 18.3 13.1–25.5
|HDmax| 28 10.1 2.8 7 13.8 12.3–15.8
|PDmin| 43 5.4 1.7 11 7.8 6.3–10.2
|PDmax| 37 5.5 2.1 9 8.2 6.2–13.4
TASstraight 79 13.4 5.1 20 20.5 16.6–28.4
Straight-line soft surface
|HDmin| 39 11.4 5.1 10 18.8 15.2–27.6
|HDmax| 28 10.4 4.3 7 16.5 12.0–21.9
|PDmin| 43 5.4 1.7 11 7.8 6.1–9.9
|PDmax| 34 5.1 2.0 9 7.8 6.0–12.0
TASstraight 78 12.9 4.4 20 19.0 15.5–22.7

Abbreviations: HDmin/max, mean difference in head minimum/maximum positions between right and left portions of the strides; PDmin/max, mean difference in pelvic minimum/maximum position between right and left portions of the strides; 75th percentile, the quarter of the highest movement asymmetry values for respective variable; n 75th percentile, number of horses in the 25% highest movement asymmetry values. Thresholds: > |6| mm for HDmin/HDmax and >|3| mm for PDmin/PDmax.

Lunge

For gait analysis on the lunge in both directions, 121 horses were analysed. The mean number of strides per trial was 56 ± 20 (range 25–178). Of the 79 horses classified as asymmetric in straight-line trot on a hard surface, 77 had trials on the lunge in both directions. Of the 35 horses classified as symmetric, in straight-line trot on a hard surface, all had trials on the lunge in both directions. Descriptive movement asymmetry values obtained in trials on the lunge for horses classified as symmetric or asymmetric are presented in Table 3.

Table 3. Movement asymmetry values on the lunge of horses classified as either asymmetric or symmetric in straight-line trot on a hard surface.

Classified asymmetric on straight line Classified symmetric on straight line
n Mean (mm) SD (mm) Mean 75th (mm) Max (mm) n Mean (mm) SD (mm) Mean 75th (mm) Max (mm)
Left circle
HDmin right 41 8.1 6.1 16.8 24.7 21 8.6 7.3 19.1 28.4
HDmin left 36 -8.4 7.2 -17.6 -32.5 14 -6.8 7.8 -17.6 -22.3
HDmax right 31 5.5 3.8 10.5 13.6 20 6.0 5.6 13.7 21.2
HDmax left 46 -6.1 5.0 -12.9 -22.0 15 -4.4 4.4 -10.8 -12.0
PDmin right 16 2.5 2.0 5.4 6.5 8 2.8 2.4 6.0 8.1
PDmin left 61 -6.5 4.3 -12.3 -17.5 27 -6.2 3.8 -10.9 -14.1
PDmax right 47 3.9 3.4 8.8 13.4 23 2.4 1.6 4.5 7.2
PDmax left 30 -2.4 2.2 -5.6 -7.2 12 -1.8 1.4 -3.6 -5.2
Right circle
HDmin right 25 6.4 6.8 16.0 27.1 14 5.5 4.7 11.5 12.6
HDmin left 52 -8.8 8.0 -19.9 -33.9 21 -8.4 6.1 -16.0 -26.4
HDmax right 43 7.8 6.7 17.3 27.2 20 5.6 3.8 10.9 14.5
HDmax left 34 -4.6 4.1 -10.6 -14.8 15 -8.7 8.2 -18.7 -29.2
PDmin right 70 7.2 4.3 13.1 16.9 31 7.7 5.0 14.1 18.6
PDmin left 7 -2.9 2.0 -5.5 -5.5 4 -3.5 2.6 -6.3 -6.3
PDmax right 24 2.1 2.3 5.2 10.3 8 2.3 1.3 4.1 4.3
PDmax left 53 -4.1 3.2 -8.5 -15.4 27 -3.5 2.6 -7.0 -9.5

Movement asymmetry values on the lunge, both directions, for the 77 horses classified as asymmetric (left) in straight-line trials on a hard surface, and (right) the 35 horses classified as symmetric. Abbreviations: HDmin/max, mean difference in head minimum/maximum positions between right and left portions of the strides; PDmin/max, mean difference in pelvic minimum/maximum position between right and left portions of the strides; SD, standard deviation; Mean 75th; mean value of the highest quarter of values; Max, highest value; n, number of trials in either direction (R or L) for that parameter by the 77 asymmetric horses and the 35 symmetric horses.

Rider-perceived sidedness

Questionnaire responses (obtained for 71 horses) are presented in Table 4. The responses were used to investigate the association between perceived sidedness and vertical movement asymmetries of the horse.

Table 4. Questionnaire response on perceived sidedness.

Question Pre-set answer options Answers expressed as % of responders
1. Do you perceive your horse as exhibiting a sidedness? If so, please grade it. No 8.5% (6 of 71)
Mild 66.2% (47 of 71)
Moderate 22.5% (16 of 71)
Severe 2.8% (2 of 71)
No perception/did not answer 0% (0 of 71)
2. Do you perceive your horse as having a weaker hind limb? No 38.0% (27 of 71)
Yes (left or right) 59.2% (42 of 71)
No perception/did not answer 2.8% (2 of 71)
3. Do you perceive your horse as leaning more on either of the reins? None 31.0% (22 of 71)
Left 35.2% (25 of 71)
Right 33.8% (24 of 71)
No perception/did not answer 0% (0 of 71)
4. Do you perceive your horse as drifting out on the circle? None 45.1% (32 of 71)
Left 25.4% (18 of 71)
Right 28.2% (20 of 71)
No perception/did not answer 1.4% (1 of 71)
5. Do you perceive yourself as having unequal sides with one side perceived as more difficult to ride in? None 45.1% (32 of 71)
Left 24.0% (17 of 71)
Right 31.0% (22 of 71)
No perception/did not answer 0% (0 of 71)

Responses to questions used to investigate association of perceived sidedness and vertical movement asymmetries. Answers based on the number of horses included (71), for question 5 an overlap of 20 answers occurred as multiple horses had the same rider, percentage reported is based on horse and not rider.

Questions where the responses of over 50% of the participants were “no” were not included in statistical analysis, since no perceived sidedness was recorded. For the questions that were not included, an equal distribution of difficulty in either direction was seen.

Association between sidedness and movement asymmetries

No associations were seen between rider-perceived sidedness in the responses to questions 1–5 and selected asymmetry parameters in straight-line trot. A statistically significant association was seen for the questionnaire response on perceived sidedness (question 1) and TAS on the lunge. Perceived sidedness and stride duration were both significant in relation to the total movement asymmetry score on the lunge for this question. Results are presented in Table 5, while plots of TAS on the lunge and the straight against rider-perceived sidedness are presented in Figs 1 and 2.

Table 5. ANOVA results for questionnaire responses tested against asymmetry parameters.

Independent variable Dependent variable p-value Stride duration p-value
Sidedness (1) TASstraight 0.38 0.06
Sidedness (1) TASlunge 0.02* 0.01**
Weak hind limb (2) PDmin 0.72 0.08
Weak hind limb (2) PDmax 0.43 0.82
Leaning on rein (3) HDmin 0.91 0.41
Leaning on rein (3) HDmax 0.44 0.74
Drift on circle (4) HDmin 0.65 0.40
Drift on circle (4) HDmax 0.48 0.71
Drift on circle (4) PDmin 0.45 0.09
Drift on circle (4) PDmax 0.61 0.79
Harder side rider (5) HDmin 0.34 0.44
Harder side rider (5) HDmax 0.60 0.76
Harder side rider (5) PDmin 0.40 0.08
Harder side rider (5) PDmax 0.67 0.74

Responses to questions 1–5 presented as independent variable and selected asymmetry parameters as dependent variable. Abbreviations: TAS, total asymmetry score; HDmin/max, mean difference in head minimum and maximum position between right and left portions of the strides; PDmin/max, mean difference in pelvic minimum and maximum position between right and left portions of the strides. P-values <0.05 are indicated by * and p-values <0.01 are indicated by **.

Fig 1. Total asymmetry score (TASstraight) in straight-line trot plotted against level of rider-perceived sidedness.

Fig 1

Responses to questionnaire question 1 on riders’ perception of the horse exhibiting a sidedness and the degree of sidedness (no, mild, moderate) plotted against total asymmetry values obtained in straight-line trials on a hard surface. First and third quartiles represented by the upper and lower parts of the boxes. Whiskers extend to the minimum and maximum value, but no longer than 1.5 times the interquartile range. The solid line corresponds to the median value and the dashed line to the mean value. Data overlaid as small dots, outliers indicated by large dots.

Fig 2. Total asymmetry score (TASlunge) from lunge trials plotted against level of rider-perceived sidedness.

Fig 2

Responses to questionnaire question 1 on riders’ perception of the horse exhibiting a sidedness and the degree of sidedness (no, mild, moderate) plotted against total asymmetry values on the lunge. First and third quartiles represented by the upper and lower parts of the boxes. Whiskers extend to the minimum and maximum value, but no longer than 1.5 times the interquartile range. The solid line corresponds to the median value and the dashed line to the mean value. Data overlaid as small dots, outliers indicated by large dots. Significant difference between groups marked with asterisk (*), no significance marked with “NS”.

On comparing groups of graded sidedness (no, mild and moderate) in the model of TAS on the lunge and sidedness, a significant difference was seen between the group “no” and both “mild” and “moderate” (no vs. moderate 0.024; no vs. mild 0.029). No significant difference was seen between the groups “mild” and “moderate” (0.899). The estimated marginal mean for the three groups was as follows: mild 1.027; moderate 1.028; no 1.023 (presented on the transformed scale).

Discussion

This study examined the prevalence of vertical movement asymmetries in a group of high-performing horses and the association between riders’ perception of horse sidedness and movement asymmetries. In accordance with previous findings in horses used for general-purpose activities [12, 15], polo horses [16], reining Quarter Horses [32] and elite eventing horses [14], the high-performing riding horses in this study displayed a high prevalence (69–70%) of vertical movement asymmetries on both hard and soft surfaces regardless of equestrian discipline, when applying commonly used thresholds. In a group of warmblood foals examined in a previous study, the prevalence of movement asymmetries were lower, with 45% of the foals measuring with asymmetry values above thresholds [21]. The difference in prevalence of movement asymmetries between foals and older horses could indicate an influence of training or an increasing cumulative risk of injuries with increasing age. Although, a prevalence comparable to the one shown in the present study has also been seen among young riding horses in their early years of training [25].

Even for the horses in this study population exhibiting movement asymmetries just above the thresholds, the magnitude of these asymmetries falls within the range reported for clinically lame horses with a positive response to diagnostic analgesia [17, 18, 33]. Consequently, 69% of the horses in this high-performing population displayed movement asymmetries that could potentially indicate a painful condition. More than one-third of the studied horses showed absolute values exceeding 12 mm for forelimb parameters and 6 mm for hind limb parameters, which is double the clinically used thresholds of the Equinosis system. Although we know that vertical movement asymmetries of the head and pelvis are highly sensitive measures to detect induced lameness [34], the specificity is unknown and we cannot say if these asymmetries represent undetected orthopedic disease. High-performing athletes have an elevated risk for both traumatic and repetitive strain injuries, but more clinical information would be needed to make claims about presence of pathology. A full clinical lameness examination, including diagnostic analgesia, would provide more insight. Also, repeated measurements over time could add information about the clinical relevance of the asymmetries since it could reveal whether the asymmetries increase or decrease with increasing workload or with a specific type of training. The question of which horse might be lame or not, is also further complicated by the fact that a bilaterally lame horse could sometimes be symmetrical on the straight and the lameness associated asymmetry might appear only during lungeing or ridden exercise.

High-performing horses often go through regular health checks, including lameness assessments by treating veterinarians or during horse inspections for fitness to compete. They are additionally managed by experienced riders or trainers. However, subjective detection of lameness is difficult for both trainers [5] and veterinarians [4], and the assessment of “fit to compete” may differ between observers [35]. One could also argue that since the horses had performed at high levels within the last six months, this would indicate that the asymmetries do not prevent performance at a high level and thus are less likely to associate with orthopedic disease. However, this does not exclude a performance-reducing and painful pathology as the cause of the asymmetries. Addressing possible underlying causes of asymmetries might still result in both enhanced performance and increased welfare for the horse.

Despite the high amplitude of vertical asymmetries measured in a large propotion of the horses, horse owners in the present study did not report any performance issues with their horse/s. The lack of reported clinical issues might either mean that the riders/owners did not detect any asymmetries or that they did not associate the asymmetry with lameness. Almost all the riders did however perceive the horses as exhibiting sidedness. I.e. almost no riders answered that they did not perceive a difference between sides. Thus the movement asymmetries recorded might be subconsciously translated into the concept of the horse having a strong or weak side, rather than potential lameness. No association between the total asymmetry score, TAS, in straight-line trot and perception of an existing sidedness as described in the different questions was seen in this study. However, a significant association was seen when modelling TAS on the lunge and perceived overall sidedness (p = 0.02). Lunging induces systematic asymmetries [12] that accentuates preexisting movement asymmetries [13]. The resulting difference in symmetry between directions, in the baseline asymmetric horse, may be what the rider feel and describe as sidedness. Laterality, in turn, as the cause of the movement asymmetries, is not supported by the results, as none of the more specific riders’ perception of sidedness questions had a significant association with movement asymmetry.

The questionnaire aimed to reflect common descriptions of how a stronger or weaker side is thought to affect ease of movement. However, the details by which each rider would truly assess and describe a weak or strong side was not covered by the questionnaire except for question 2, where the description varied among riders. It is uncertain whether the questionnaire succeeded in quantifying the perceived sidedness of the horse and reflected potential sidedness correctly, or whether e.g. the rider’s own laterality influenced the results, especially since some riders rode several horses. The riders recall, or potential lack of recall, of a perceived sidedness in association to the different movements/questions could also have influenced the results. A collection protocol, with the opportunity to ride in connection with answering the questionnaire would be more favourable, also in combination with gait analysis under rider. This approach would have amended a shortcoming with the current study setup where the riders’ perceived sidedness were based on an overall perception and probably of the horse in a generally more warmed up condition than during the gait analysis trot up.

This study has several limitations of which some are already mentioned and discussed above. Two additional limitations are, first, the study was performed on only a small sample of eventing horses, since the small population of eventing horses in Sweden entailed difficulties in recruiting a substantial number of horses in this category. Secondly, a consistent or randomised order for the different conditions would be beneficial, as a longer warm-up might reduce or increase movement asymmetries.

Conclusions

Vertical movement asymmetries were present in a high proportion (69.3%) of a population of high-performing horses in full athletic condition participating, in dressage, show jumping or eventing. In many of the horses, movement asymmetries were of the same magnitude as reported in horses with confirmed clinical lameness. No clear-cut associations were observed between riders’ perception of sidedness and the vertical movement asymmetry values, indicating that rider-perceived sidedness is not a determinant of vertical movement asymmetry. Longitudinal studies on movement asymmetries in relation to training intensity and full clinical examinations are desired as further research to determine whether movement asymmetries indicate an animal welfare problem.

Supporting information

S1 Text. Rider-perceived questionnaire.

Pdf file containing the questionnaire about rider-perceived sidedness.

(PDF)

pone.0308061.s001.pdf (280.2KB, pdf)
S2 Text. Results for subset of horses.

File containing descriptive and statistical results for the subset of horses with questionnaire responses collected in conjunction with gait analysis.

(PDF)

pone.0308061.s002.pdf (397.8KB, pdf)
S3 Text. Background questionnaire.

Pdf file containing the background questionnaire.

(PDF)

pone.0308061.s003.pdf (122.6KB, pdf)
S1 File. Data sets.

Excel book containing sheets with the data sets used. Sheet ‘Straight-line Hard Surface’, ‘Straight-line Soft Surface’ and ‘Lunge’ contains data from included horses for each condition.

(XLSX)

pone.0308061.s004.xlsx (84.5KB, xlsx)
S2 File. Data set used for statistical analysis.

Microsoft excel file containing data used in statistical analyses.

(XLSX)

pone.0308061.s005.xlsx (27.9KB, xlsx)

Data Availability

All relevant data are within the manuscript and its Supporting Information files

Funding Statement

This study was founded by the Swedish-Norwegian Foundation for Equine Research (https://hastforskning.se/in-english/), project number H-17-47-286, awarded to MR and EH. The funders of the study had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Decision Letter 0

Rebecca Lee Smith

20 Mar 2024

PONE-D-23-43274Prevalence of movement asymmetries in high-performing horses perceived as free from lameness by the owner and riders’ perception of horse sidednessPLOS ONE

Dear Dr. Zetterberg,

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Reviewer #2: Yes

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Reviewer #1: It was a pleasure to read a well-written manuscript describing a well-designed study.

However, I would strongly encourage you to remove the ‘handedness data’ that were not acquired at the time of gait analysis. I ask clients questions on a daily basis about handedness – they struggle to remember left and right, even having ridden the horse the previous day. So even data collected at the time of examination have doubts about accuracy. Data collected at a time remote from the gait assessment cannot be considered to be accurate, particularly for riders who are riding several horses a day.

I would also strongly recommend including a statement in the limitations of the study about the potential unreliable nature of contemporaneous rider recall.

Title – Are you differentiating between owners and riders – please clarify here & in the manuscript.

Line 79 We do not know that lameness is present in high performing equine athletes from a variety of published studies.

And we also know that judges miss lameness – also documented previously.

Horse inspections are only in hand in straight lines therefore these so-called veterinary inspections, correctly called horse inspections, can miss lameness. Moreover, the decision is made by the Ground Jury, not the attending veterinarian, and the criterion is ‘fit to compete’ not the absence of lameness. The veterinarian merely supplies advise to the Ground Jury when requested to do so. And if you ever watch the horse inspection (‘trot up’) at an international showjumping competition you will realise that is a token inspection, with the majority of horses being presented very badly, making it virtually impossible to make an accurate assessment.

Please amend the text accordingly.

Ridden exercise - more likely to show lameness – there are several studies that have shown that the absence of lameness in straight lines does not preclude lameness either on the lunge or when ridden. It must also be borne in mind that the absence of measurable asymmetry does not preclude lameness when present bilaterally. If you investigate horses presented for evaluation of the reason for poor performance this is a not uncommon scenario which needs to be recognised.

Please amend the text accordingly.

Line 110 & elsewhere lungeing (not lunging – this word is commonly not spelt correctly – the ‘g’ is soft in pronunciation because of the ‘e’)

Line183 both in straight lines and on the lunge

Line 200 '12% within a year and 8% one year after the gait analysis' Those responses should probably not be included – see above.

Line 240 as asymmetric

Tables 2 & 3 I suggest it would make more biological sense if all results were presented to no more than 1 decimal place

Table 5 Do not present p-values to more than 2 decimal places

Stride duration p-value - no more than 2 decimal places

Please mention * in legend

Lines 343- 345 – I would suggest that you include mention of the fact that a full clinical examination should include ridden exercise and should also include the use of a pain-analysis tool, such as the Ridden Horse Pain Ethogram. As a clinician you can only determine the influence of a gait variant on overall performance if you evaluate the horse doing what it is supposed to do. For example, a Prix St George dressage horse may be completely comfortable in working trot, but may struggle to perform tempi changes because of underlying discomfort associated with the measured gait asymmetry. On the other hand if the asymmetry is not associated with pain the horse may be able to perform all movements easily.

The observations in your study are really important to be aware of in pre-purchase examinations – another reason why it is important to discuss the importance of ridden exercise and evaluation of behaviour potentially reflecting discomfort.

Line 346 ‘High-performing horses are regularly assessed for lameness by veterinarians at competitions’ – see previous comments about the role of veterinarians in the disciplines of dressage, showjumping and eventing. It is only in endurance riding that the veterinarians make decisions.

Please amend the text accordingly.

Line 352 please make sure that this refers to experimentally induced lameness

Line 368 '…….indicating that the vertical asymmetries recorded did not impair their performance' - You cannot conclude that - if the horses did have pain-induced asymmetry their performance may be improved by removal of this. Diagnosis and appropriate treatment usually results in better performance - I see this regularly!

It has also been demonstrated that horses with higher Ridden Horse Pain Ethogram scores perform less well at a variety of levels and in a variety of disciplines than horses with no detectable lameness and low ethogram scores.

Line 372 A good rider may conceal lameness by continuously making subtle adjustments or accentuate lameness by asking a horse to work harder

A limitation of the study is that horses were not assessed ridden.

Line 405 among riders (between 2, among >2)

Line 422 Please see previous comments about ridden assessment and the use of pain recognition tools, e.g., the RHpE

Reviewer #2: I think this is a valuable and really interesting line of enquiry. I have only minor comments and a suggestion re the discussion as follows:

Line 51: Please consider referring to a previous definition of lameness within the introduction. If the reader interprets 'lameness' as 'movement asymmetry' for example, line 51 where you say "it is difficult to exclude lameness as a cause of movement asymmetries in these horses" would not make sense. As I read the introduction, I had to assume your definition of lameness, was some movement abnormality resulting from pain (?). Or replace the word 'lameness' with 'pathology?' in line 51?

Line 81: should therefore 'be more likely to be noticed'

Line 91: 3 star post the classification change in 2019?

Line 97: Could the questionnaire on horse history be provided?

Line 110: Re the lunge condition - 10 m diameter? Was this standardised?

Line 134: Consider stating here that the aim was 25 or 20 strides following removal of strides that couldn't be used. Later, when we read how the data were 'cleaned' it led me to wonder how many useable strides were left, until I realised that 25/20 was the aim POST removal of outliers and anomalous strides.

Line 166 - 170: Why is HDmin and HDmax/2 but not PDmin and max?

Line 180: should it not read 'Ime4' not Imer?

Line 221: I think having 20% of riders not complete the questionnaire on day of testing is a limitation that should be pointed out. I would be interested to know if removing these riders changed the outcome of the stats.

Table 2: Minor detail but several results are reported to 1 decimal place rather than 2 (the majority). In fact I would query whether you can report to 1/100th of a mm?

Line 342: why are the 6 and 12 in square brackets?

Line 360: should read 'highlights' not highlight.

Discussion - Whilst I appreciate you must present the data and provide impartial discussion, I was not clear whether you were suggesting that a large number of competition horses are actually lame, or that we need to rethink these thresholds, or that we don't yet know? If it is that we don't yet know, perhaps a more explicit statement could be added that addresses how this current work fits in to the current debate about what is a normal level of asymmetry? I think what should also be acknowledged is that the horses were not tested in a ridden situation and therefore you don't know if the asymmetry seen in the unloaded condition has any relationship to asymmetries that might occur in the ridden (and warmed up) condition. Perhaps a question too far for the questionnaire (!) but it would have been interesting to know if riders perceive sidedness pre AND post warm up - perhaps part of warm up for the individual is to achieve symmetry.

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PLoS One. 2024 Jul 30;19(7):e0308061. doi: 10.1371/journal.pone.0308061.r002

Author response to Decision Letter 0


2 May 2024

Response to Reviewers PONE-D-23-43274

Lines specified below refer to the file “Revised Manuscript with Track Changes”

Reviewer #1: It was a pleasure to read a well-written manuscript describing a well-designed study.

Thank you for all the valuable suggestions and feedback to improve our manuscript.

However, I would strongly encourage you to remove the ‘handedness data’ that were not acquired at the time of gait analysis. I ask clients questions on a daily basis about handedness – they struggle to remember left and right, even having ridden the horse the previous day. So even data collected at the time of examination have doubts about accuracy. Data collected at a time remote from the gait assessment cannot be considered to be accurate, particularly for riders who are riding several horses a day.

I would also strongly recommend including a statement in the limitations of the study about the potential unreliable nature of contemporaneous rider recall.

Answer: We agree that the time difference between the gait analysis and the sidedness questionire response is a limitation. We share your concern that this might influence the results and therefore performed a test where we remove these horses from the analysis. We didn´t see any changes in the results (when excluding these horses). These results have been added as a supporting file, S4. Due to the lack of difference with these horses removed, we decided to include horses with a time difference between the gait analysis and the questionnaire response.

As you point out, the recollection for most persons not that excellent. Also, the influence of the rider's own laterality and perceived position/proprioception might influence the responses in the sidedness questionnaire. It would be more accurate if the riders answered these questions during riding and also on multiple occasions. For this study setup, this was not feasible, but we still wanted to try to capture the perceived sidedness that most riders feel (and that is described) and see if there was a clear association with vertical asymmetries. From this study, we want to show that there is not a clear association at this level. However, there might be an association if you would do a more in-depth study where you would study the riders laterality, what the riders are perceiving – as the perception might not be a reflection on reality, and also over time if the perceived sidedness changes and relation to other factors (training intensity, pasture changes etc).

The supporting info and why these 20% were included are addressed in line 236-238. A sentence have also been added to address the uncertainty of the riders recall, see line 451-452.

Title – Are you differentiating between owners and riders – please clarify here & in the manuscript.

Answer: Yes, the questionnaire of sidedness was answered by the riders (not necessarily the same person as the owner). While the owner was responsible for the horse and its participation.

This is clarified in material and methods, line 110, and the title is changed

Line 79 We do not know that lameness is present in high performing equine athletes from a variety of published studies.

And we also know that judges miss lameness – also documented previously.

Horse inspections are only in hand in straight lines therefore these so-called veterinary inspections, correctly called horse inspections, can miss lameness. Moreover, the decision is made by the Ground Jury, not the attending veterinarian, and the criterion is ‘fit to compete’ not the absence of lameness. The veterinarian merely supplies advise to the Ground Jury when requested to do so. And if you ever watch the horse inspection (‘trot up’) at an international showjumping competition you will realise that is a token inspection, with the majority of horses being presented very badly, making it virtually impossible to make an accurate assessment.

Please amend the text accordingly.

Answer: As you point out, the circumstances under which the horse inspections take place are indeed suboptimal. The subjective assessments are limited and we have tried to suggest that the regular checks by experienced owners and riders and horse inspection should give a higher possibility of an abnormality being detected but as you highlight we also believe this isn´t always the case. This is in comparison to lower-level horses with e.g. hobby owners that usually are not looked at regularly by professionals or by veterinarians.

For eventing horses at a high level have a high prevalence of asymmetries been shown. There are also some studies which assess lameness subjectively in high-level horses but to our knowledge no study based on objective measurments have been done.

According to Swedish law should all horse inspections be carried out by a veterinarian and in FEI-organised competitions there should always be an official veterinarian included in the decision.

We have tried to clarify the section. See lines 81-86.

Ridden exercise - more likely to show lameness – there are several studies that have shown that the absence of lameness in straight lines does not preclude lameness either on the lunge or when ridden. It must also be borne in mind that the absence of measurable asymmetry does not preclude lameness when present bilaterally. If you investigate horses presented for evaluation of the reason for poor performance this is a not uncommon scenario which needs to be recognised.

Please amend the text accordingly.

Answer: We agree that for achieving a good assessment of a horse with poor performance problems and other indications of lameness should the evaluation be extensive, including e.g. ridden exercise. This was not in the scope of this study. Some of the horses classified symmetric in the straight line trials could have shown abnormal asymmetries on the circle indicating a bilateral asymmetry, and it would have been interesting to study how each horse looked on the circle compared to the straight lines but this was not possible for this study. And as we have not examined these horses for lameness it would be difficult to draw any conclusions from this.

We have added a section regarding the classification as “symmetric” in relation to bilateral lameness and lungeing and ridden exercise, see lines 380-382.

Line 110 & elsewhere lungeing (not lunging – this word is commonly not spelt correctly – the ‘g’ is soft in pronunciation because of the ‘e’)

Answer: thank you, this has now been corrected.

Line183 both in straight lines and on the lunge

Answer: thank you, this has now been corrected.

Line 200 '12% within a year and 8% one year after the gait analysis' Those responses should probably not be included – see above.

Answer: We thought about this and tested if the exclusion of this data had an impact on the results. As the results don´t change when these horses were removed we have chosen to keep all the horses where the rider responded to the sidedness questionnaire. We have tried to clarify this, see lines 236-238, see also the supporting file for the results presented without these 20% of horses.

Line 240 as asymmetric

Answer: Thank you, this has now been corrected.

Tables 2 & 3 I suggest it would make more biological sense if all results were presented to no more than 1 decimal place

Answer: The results have now all been rounded to one decimal place

Table 5 Do not present p-values to more than 2 decimal places

Stride duration p-value - no more than 2 decimal places

Please mention * in legend

Answer: The p-values have been rounded to 2 decimal places and a description for * has been added.

Lines 343- 345 – I would suggest that you include mention of the fact that a full clinical examination should include ridden exercise and should also include the use of a pain-analysis tool, such as the Ridden Horse Pain Ethogram. As a clinician you can only determine the influence of a gait variant on overall performance if you evaluate the horse doing what it is supposed to do. For example, a Prix St George dressage horse may be completely comfortable in working trot, but may struggle to perform tempi changes because of underlying discomfortassociated with the measured gait asymmetry. On the other hand if the asymmetry is not associated with pain the horse may be able to perform all movements easily.

The observations in your study are really important to be aware of in pre-purchase examinations – another reason why it is important to discuss the importance of ridden exercise and evaluation of behaviour potentially reflecting discomfort.

Answer: We agree that we don’t know that the presence of vertical movement asymmetries equals lameness for these horses. We have tried to clarify this, see line 372.

Line 346 ‘High-performing horses are regularly assessed for lameness by veterinarians at competitions’ – see previous comments about the role of veterinarians in the disciplines of dressage, showjumping and eventing. It is only in endurance riding that the veterinarians make decisions.

Please amend the text accordingly.

Answer: According to Swedish law (Djurskyddsförordningen 1988:539), (which is the location for this study), should all horses competing at regional competitions be checked by a veterinarian before competitions.

For competitions organized by the FEI the decision must be based on the opinion of the veterinarian delegate, and a veterinarian needs to be on the inspection panel, but as you point out has the president of the grand jury the casting vote.

We have tried to clarify the focus in these “assessments”, see lines 383-388.

Line 352 please make sure that this refers to experimentally induced lameness

Answer: this has been clarified in the text. See line 371.

Line 368 '…….indicating that the vertical asymmetries recorded did not impair their performance' - You cannot conclude that - if the horses did have pain-induced asymmetry their performance may be improved by removal of this. Diagnosis and appropriate treatment usually results in better performance - I see this regularly!

It has also been demonstrated that horses with higher Ridden Horse Pain Ethogram scores perform less well at a variety of levels and in a variety of disciplines than horses with no detectable lameness and low ethogram scores.

Answer: We agree that the phrasing was not optimal, we have worked on the discussion, see section 390-395.

Line 372 A good rider may conceal lameness by continuously making subtle adjustments or accentuate lameness by asking a horse to work harder

A limitation of the study is that horses were not assessed ridden.

Answer: We have added and rearranged in the discussion.

Line 405 among riders (between 2, among >2)

Answer: thank you, this has now been corrected.

Line 422 Please see previous comments about ridden assessment and the use of pain recognition tools, e.g., the RHpE

Answer: We agree, it would be beneficial to study these vertical movement asymmetries in combination to a full clinical examination, where for example ridden exercises are conducted and in connection to different pain assessment tools.

Reviewer #2: I think this is a valuable and really interesting line of enquiry. I have only minor comments and a suggestion re the discussion as follows:

Thank you for taking the time to review our manuscript.

Line 51: Please consider referring to a previous definition of lameness within the introduction. If the reader interprets 'lameness' as 'movement asymmetry' for example, line 51 where you say "it is difficult to exclude lameness as a cause of movement asymmetries in these horses" would not make sense. As I read the introduction, I had to assume your definition of lameness, was some movement abnormality resulting from pain (?). Or replace the word 'lameness' with 'pathology?' in line 51?

Answer: Thank you, we have added to the sentence to hopefully clarify this, see line 57.

Line 81: should therefore 'be more likely to be noticed'

Answer: the section have been rewritten, see section starting in line 80.

Line 91: 3 star post the classification change in 2019?

Answer:We have tried to clarify this, the requirements were set to 3* for both before and after the change but as you point out is there a lower level after 2019..

Line 97: Could the questionnaire on horse history be provided?

Answer: We have added the background questionnaire, see supporting info S5.

Line 110: Re the lunge condition - 10 m diameter? Was this standardised?

Answer: The handlers were instructed to use a 10 m circle and this was adjusted if obviously too small or big but it was not standardized to be exactly 10m using e.g. fencing. This has been rewritten.

Line 134: Consider stating here that the aim was 25 or 20 strides following removal of strides that couldn't be used. Later, when we read how the data were 'cleaned' it led me to wonder how many useable strides were left, until I realised that 25/20 was the aim POST removal of outliers and anomalous strides.

Answer: thank you, we have tried to clarify this.

Line 166 - 170: Why is HDmin and HDmax/2 but not PDmin and max?

Answer: The total range of motion of the head increases with forelimb lameness, making the asymmetries (HDmin/HDmax) approximatly double the size compared to pelvic motion asymmetry (PDmin/PDmax). Therefore head movement asymmetries were divided with two when combined with pelvic motion asymmetries to ensure equal contribution of each into the combined measure.

Line 180: should it not read 'Ime4' not Imer?

Answer: The package used in R is called lme4 whereas the function used for the data is called lmer (found in the package lme4).

Line 221: I think having 20% of riders not complete the questionnaire on day of testing is a limitation that should be pointed out. I would be interested to know if removing these riders changed the outcome of the stats.

Answer: We have added the results of the statistic tests when these horses were removed as a supporting file, see S4. We thought about this as well but as we believed that the perceived sidedness ought to be more stable, at least in older horses, we included all horses and when we testet to exclude them the results were the same.

Table 2: Minor detail but several results are reported to 1 decimal place rather than 2 (the majority). In fact I would query whether you can report to 1/100th of a mm?

Answer: we have shifted the decimal place. Note that the results are presented as mm but are corrected to the range of motion in the horse and thereby not actual mm in reality.

Line 342: why are the 6 and 12 in square brackets?

Answer: the vertical straight lined (|nr|) around 6 and 12 are to describe that the number is an absolute value, we do not take into consideration if the asymmetry is to the left or right (giving negative or positive values).

Line 360: should read 'highlights' not highlight.

Answer: thank you, this has been corrected.

Discussion - Whilst I appreciate you must present the data and provide impartial discussion, I was not clear whether you were suggesting that a large number of competition horses are actually lame, or that we need to rethink these thresholds, or that we don't yet know? If it is that we don't yet know, perhaps a more explicit statement could be added that addresses how this current work fits in to the current debate about what is a normal level of asymmetry?

Answer: We have substantially rearranged in the discussion to try to make it easier to follow the line of thought and make the discussion clearer. As you point out, this is a difficult discussion, we do not know the significance of the vertical movement asymmetries in populations of horses perceived as sound by the owners. We believe the thresholds can be of some help in the clinical situation but they do not show in black and white if the horses movement asymmetry is caused by pain or not, especially in horses with no other signs of lameness. We do however need to keep in mind that other signs might be difficult to perceive as well, as the horses are experts at hiding pain. The high prevalence of horses with big amplitude differences is concerning but we do not know the specificity of the asymmetries to pain. At this stage, we believe th

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Decision Letter 1

Rebecca Lee Smith

30 May 2024

PONE-D-23-43274R1Prevalence of movement asymmetries in high-performing riding horses perceived as free from lameness and riders’ perception of horse sidednessPLOS ONE

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Reviewer #1: The revised version of this paper presents a more balanced picture of the study results and limitations of the study. I would suggest that it needs to be put into a broader perspective of what has been reported from other countries. I still think that there are some additional points which need addressing.

I also think that the authors need to be rather more transparent. This is a worrying situation with such a high percentage of potentially lame horses. The group, along with other groups, have rightfully been championing the use of objective gait evaluation. But this study highlights that either our so-called cut off points for differentiating lameness and non-lame horses are highly inaccurate, or that there is a high percentage of actively competing sports horses that are lame. This needs to be addressed in a straightforward manner in my opinion.

In saying that in my clinical experience there is a subset of competition horses that have low grade lameness (for which we have a diagnosis) and with careful management stay the same year in year out. There is another subset with a similar low-grade lameness (for which we have a diagnosis) in which unquestionably the horse’s performance is compromised (we know from analysis of competition results and, when they have been educated, the riders become aware of changes in ‘rideability’ – responsiveness to cues, which they might have previously ignored [ignorance is bliss]); then there is a third subset that if you evaluate them on one day they will be mildly lame but if you follow them over time the lameness gets slowly worse.

Additional specific points to be addressed:

Line 33 No clear association was found between rider-perceived sidedness and the vertical movement asymmetry values, indicating that laterality is so far not a determinant for vertical movement asymmetry. How can you conclude laterality is not a is not a determinant of vertical movement asymmetry based on no clear association between rider perceived sidedness and movement asymmetry measurements? And the mixture of the terms laterality and sidededness creates confusion.

Line 35 - diagnostic anaesthesia is the way with reasonable certainty to determine if there is pain causing asymmetrical movement.

Line 83-86 This sentence is not grammatically correct. Please rephrase. Moreover it has been shown that trainers are rather poor at recognising lameness, even with training – as you cite in ref 5.

Line 95 There are 2 publications which have used objective gait analysis in addition to those in which subjective observations have been made. It is therefore not reasonable to say 'unknown'.

Contino, E.; Daglish, J.; Kawcak, C. The prevalence of lameness in FEI athletes and its correlation to performance. Proc. Am. Assoc. Eq. Pract. 2023, 69, 369-370.

Scheidegger, M.D.; Gerber, V.; Dolf, G.; Burger, D.; Flammer, A.; Ramseyer, A. Quantitative Gait Analysis before and after a Cross-country Test in a Population of Elite Eventing Horses. J. Equine Vet. Sci. 2022, 117, 104077

Line 123 presumably this is 10m diameter. Please add

Line 137 I realise that this may standard practice, but it (the outliers) could be a genuine biological observation reflecting varying discomfort - in my clinical experience it is not uncommon to see horses that very in the severity of lameness shown from stride to stride - which is why it is important to watch a horse for long enough so that you are aware of any spontaneous fluctuations in gait. I think this merits mention in the Discussion.

Line 138- 140 This is obviously required!

Line 229 varied among horses

Line 232 soft surface

Line 238 Total population dressage n=47, 38.2%; SJ n=61, 49.6%; E n=15, 12.2%

Responders (n=71) - much higher % of event (n=15) riders (100%), & possibly dressage (n=26) riders versus SJ (n=30) - how might that have influenced the overall results?

I still question the whole value of inclusion of data regarding sidedness – which relies on rider memory – accurate description by a rider competing the questionnaire for > 1 horse - reliance on rider perceptions – the fact that so-called sidedness could be related to a variety of factors – the presence of primary equine pain, the effect of the tack fit (on both horse & rider), the effect of rider position and force distribution, variability in rider skill level (yes even at these levels of competition), the variance in ability of rider’s to describe what they have just felt (I question riders on a daily basis), and what riders assume is normal (which may not be normal)!

Line 365 While recognising that there are variations among people's ability to detect and grade lameness to put your results into more perspective I think that you should also cite other studies that have evaluated horses subjectively that were considered by riders to be working comfortably.

Line 384 veterinarians

Line 397 measurements

Line 453 VERY common in my experience! One of very many myths perpetuated in the equestrian world.

Line 449- 451 good point

Line 452 - particularly for those riders who filled in a questionnaire for > 1 horse

It might have been helpful to have had additional questions in the questionnaire - e.g., do you have symmetrical rein (or does the horse lean on one rein); does the horse feel similar in rising trot on the left and right diagonals; does the horse put you on one diagonal preferentially; if you ride on the correct diagonal in rising trot, does the horse feel different on the left and right reins?

Line 475 please be consistent in the use of terminology - if you mean sidedness then say that rather than introducing laterality which creates confusion.

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PLoS One. 2024 Jul 30;19(7):e0308061. doi: 10.1371/journal.pone.0308061.r004

Author response to Decision Letter 1


12 Jul 2024

Response to reviewer PONE-D-23-43274R1

Reviewer #1: The revised version of this paper presents a more balanced picture of the study results and limitations of the study. I would suggest that it needs to be put into a broader perspective of what has been reported from other countries. I still think that there are some additional points which need addressing.

Answer: We aim to primarily compare our findings with other studies that employ the same objective methods to measure asymmetry. We have included references of asymmetries in both polo horses, riding horses and Quarter horses, which were indeed previously missing from our text.

I also think that the authors need to be rather more transparent. This is a worrying situation with such a high percentage of potentially lame horses. The group, along with other groups, have rightfully been championing the use of objective gait evaluation. But this study highlights that either our so-called cut off points for differentiating lameness and non-lame horses are highly inaccurate, or that there is a high percentage of actively competing sports horses that are lame. This needs to be addressed in a straightforward manner in my opinion.

Answer: We agree that the high percentage of asymmetries is indeed a concerning issue. Head and pelvic vertical movement asymmetry are highly sensitive indicators of forelimb and hindlimb lameness. However, the clinical specificity of these asymmetry thresholds is currently unknown. It is essential to investigate the prevalence of these asymmetries in different horse populations and to determine the specificity of these "lameness thresholds" to establish their potential use as a screening tool for lameness.

With the current knowledge, we do not believe it is possible to define cut-off values for differentiating between lame and non-lame horses. This is due to the significant overlap in absolute asymmetry values among a large proportion of horses in this study (and other studies observing asymmetries) and studies of horses with lameness confirmed through diagnostic analgesia (Maliye et al., 2015, 2016; Persson-Sjodin et al., 2023). We have in our clinical experience also observed that in some horses, small asymmetries are significant, while in others, consistent larger asymmetries do not change over time, do not increase with different training intensities, or improve with rest. The latter could potentially indicate non-pain-related asymmetries.

This study aimed to describe the prevalence of movement asymmetries and to investigate other factors associated with asymmetries, such as sidedness, in high-performing horses. It is likely that some, or even a majority, of horses with asymmetries twice the magnitude of the “threshold” used by the Lameness Locator are indeed lame and indicate a potential welfare issue. However, without systemic or local analgesic testing, we cannot confirm this definitively.

In saying that in my clinical experience there is a subset of competition horses that have low grade lameness (for which we have a diagnosis) and with careful management stay the same year in year out. There is another subset with a similar low-grade lameness (for which we have a diagnosis) in which unquestionably the horse’s performance is compromised (we know from analysis of competition results and, when they have been educated, the riders become aware of changes in ‘rideability’ – responsiveness to cues, which they might have previously ignored [ignorance is bliss]); then there is a third subset that if you evaluate them on one day they will be mildly lame but if you follow them over time the lameness gets slowly worse.

Answer: We fully agree that low-grade asymmetry or lameness can have varying implications on different horses. Given the high prevalence of asymmetry observed in our study, subjecting all horses with low-grade asymmetry to invasive diagnostic analgesia may not be the best approach, as it is invasive, painful, and carries certain risks. We believe that the key to interpreting the significance of low-grade movement asymmetry in individual horses lies in monitoring them over time. This would help us understand how they respond to rest and training, and how the lameness affects their performance

Additional specific points to be addressed:

Line 33 No clear association was found between rider-perceived sidedness and the vertical movement asymmetry values, indicating that laterality is so far not a determinant for vertical movement asymmetry. How can you conclude laterality is not a is not a determinant of vertical movement asymmetry based on no clear association between rider perceived sidedness and movement asymmetry measurements? And the mixture of the terms laterality and sidededness creates confusion.

Answer: Thank you for pointing this confusion out. We have changed the terminology to “sidedness” in both the abstract and conclusion.

Line 35 - diagnostic anaesthesia is the way with reasonable certainty to determine if there is pain causing asymmetrical movement.

Answer: We agree that conducting a full lameness exam on all horses in the study would have been highly valuable. However, due to financial limitations and ethical concerns—such as performing injections and the risk of side effects, on horses perceived as healthy by their owners—this was not feasible. With the emergence of tools like mobile apps for gait analysis, where owners can record their own horses, there is potential for more longitudinal studies on large populations of horses that may address some of our research questions in the future. Additionally, we have added “local or systemic analgesic testing” in the sentence.

Line 83-86 This sentence is not grammatically correct. Please rephrase. Moreover it has been shown that trainers are rather poor at recognising lameness, even with training – as you cite in ref 5.

Answer: The sentence has been grammatically corrected. We agree regarding the poor recognition of lameness by trainers. However, compared to horses at lower levels that probably undergo even less scrutiny (not competing or frequently observed by trainers and judges), one might expect a higher probability of detecting lameness in high-performing horses, due to the increased number of opportunities for scrutiny.

Line 95 There are 2 publications which have used objective gait analysis in addition to those in which subjective observations have been made. It is therefore not reasonable to say 'unknown'.

Answer: Thank you, this was an unfortunate choice of words, we have rewritten the sentence to be more specific.

Contino, E.; Daglish, J.; Kawcak, C. The prevalence of lameness in FEI athletes and its correlation to performance. Proc. Am. Assoc. Eq. Pract. 2023, 69, 369-370.

Scheidegger, M.D.; Gerber, V.; Dolf, G.; Burger, D.; Flammer, A.; Ramseyer, A. Quantitative Gait Analysis before and after a Cross-country Test in a Population of Elite Eventing Horses. J. Equine Vet. Sci. 2022, 117, 104077

Line 123 presumably this is 10m diameter. Please add

Answer: Thank you, this has been added to the sentence.

Line 137 I realise that this may standard practice, but it (the outliers) could be a genuine biological observation reflecting varying discomfort - in my clinical experience it is not uncommon to see horses that very in the severity of lameness shown from stride to stride - which is why it is important to watch a horse for long enough so that you are aware of any spontaneous fluctuations in gait. I think this merits mention in the Discussion.

Answer: Thank you, this is a valid point. We acknowledge that some outliers may genuinely reflect discomfort in certain individuals and emphasize the importance of observing horses over extended periods to capture the continuity of their motion. In clinical cases, individual scrutiny allows for manual inclusion or exclusion of strides based on suspected lameness. However, when measuring a large population of horses, it is crucial to establish a standardized approach to handling data. It is also important to critically assess trial quality, such as considering whether handlers are affecting the horse's head or if external factors like passing tractors are temporarily influencing measurements. These considerations should be addressed prior to conducting any analysis of the results.

Many outliers, especially those related to head movement, often correspond to horses tossing their heads rather than indicating lameness. The outlier removal process used here does not eliminate recurring strides with more extreme values. As you point out, it is important to (watch)/measure the horses for a sufficient number of strides to capture the continuity of their motion. This approach ensures that the outlier removal does not inadvertently exclude recurrent higher values, even if the severity varies among strides. The system consistently removes extreme values that are not recurring, but as you highlight, it is dependent on collecting a sufficient number of strides. Additionally, we recognize that inter-stride variability tends to decrease with higher degrees of lameness.

Our study primarily aimed to describe the study population. These points are indeed valuable but more suited for a detailed discussion on interpreting measures in clinical settings for individual horses. Such discussions delve deeper than the scope of our current study objectives.

Line 138- 140 This is obviously required!

Answer: We agree, it is important to know how the horses behaved during the data collection for the interpretation of the data.

Line 229 varied among horses

Answer: Thank you, this has now been changed.

Line 232 soft surface

Answer: Thank you, this has now been changed.

Line 238 Total population dressage n=47, 38.2%; SJ n=61, 49.6%; E n=15, 12.2%

Responders (n=71) - much higher % of event (n=15) riders (100%), & possibly dressage (n=26) riders versus SJ (n=30) - how might that have influenced the overall results?

I still question the whole value of inclusion of data regarding sidedness – which relies on rider memory – accurate description by a rider competing the questionnaire for > 1 horse - reliance on rider perceptions – the fact that so-called sidedness could be related to a variety of factors – the presence of primary equine pain, the effect of the tack fit (on both horse & rider), the effect of rider position and force distribution, variability in rider skill level (yes even at these levels of competition), the variance in ability of rider’s to describe what they have just felt (I question riders on a daily basis), and what riders assume is normal (which may not be normal)!

Answer: One reason for the lower prevalence of responses in the Show Jumping (SJ) section is that many SJ horses were measured before the implementation of the sidedness questionnaire, whereas eventing horses were measured towards the end of the study when all riders were asked to complete the questionnaire. Since only horses with completed sidedness questionnaires were modeled in relation to their asymmetries, the results should not be influenced by who filled out the questionnaire. However, a limitation arises from the smaller number of eventing horses compared to dressage and SJ horses.

We acknowledge that perceived sidedness in horses may be influenced by various factors. Nonetheless, we aimed to address the argument that asymmetries could be explained solely by a perceived sidedness. Given that these are elite riders, their perception of sidedness should be based on substantial equestrian experience. Nevertheless, we do recognize instances where different riders may perceive a horse's sidedness differently, indicating a need for further investigation in this area.

Previous studies on sidedness have shown a significantly unequal proportion of left vs. right-sidedness, whereas in our study and other population studies, the proportion of left vs. right movement asymmetries is more balanced. This observation could suggest fewer associations to sidedness in our findings.

This study represents an initial exploration of the association between vertical asymmetries and riders' perceived sidedness in high-performing horses. The study design has several areas for potential improvement, which we have attempted to discuss. While it is unfortunate that no association between rider questionnaires and asymmetry was identified, we believe that including negative results is crucial. This approach aligns with the scope of PLOS One, and we maintain that negative results contribute to advancing knowledge and avoiding wasted effort.

Line 365 While recognising that there are variations among people's ability to detect and grade lameness to put your results into more perspective I think that you should also cite other studies that have evaluated horses subjectively that were considered by riders to be working comfortably.

Answer: Since we know the agreement between visual assessment and objective methods are low we wanted to focus on studies using objective methods.

Line 384 veterinarians

Answer: Thank you, this has been changed.

Line 397 measurements

Answer: The sentence has been rewritten.

Line 453 VERY common in my experience! One of very many myths perpetuated in the equestrian world.

Line 449- 451 good point

Answer: Here, we might also need to consider the influence of time. A rider with significant motor laterality in their own body may gradually influence the horse's sides over time to mirror the rider's own sidedness.

Line 452 - particularly for those riders who filled in a questionnaire for > 1 horse

Answer: Good point, we have added this to the sentence

It might have been helpful to have had additional questions in the questionnaire - e.g., do you have symmetrical rein (or does the horse lean on one rein); does the horse feel similar in rising trot on the left and right diagonals; does the horse put you on one diagonal preferentially; if you ride on the correct diagonal in rising trot, does the horse feel different on the left and right reins?

Answer: We agree that it would have been interesting to further investigate the rider perceived sidedness with additional questions and these are excellent suggestions.

Line 475 please be consistent in the use of terminology - if you mean sidedness then say that rather than introducing laterality which creates confusion.

Answer: Thank you, we have changed to sidedness.

Attachment

Submitted filename: Response to Reviewers.docx

pone.0308061.s007.docx (23.2KB, docx)

Decision Letter 2

Rebecca Lee Smith

17 Jul 2024

Prevalence of movement asymmetries in high-performing riding horses perceived as free from lameness and riders’ perception of horse sidedness

PONE-D-23-43274R2

Dear Dr. Zetterberg,

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Reviewers' comments:

Acceptance letter

Rebecca Lee Smith

22 Jul 2024

PONE-D-23-43274R2

PLOS ONE

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Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Text. Rider-perceived questionnaire.

    Pdf file containing the questionnaire about rider-perceived sidedness.

    (PDF)

    pone.0308061.s001.pdf (280.2KB, pdf)
    S2 Text. Results for subset of horses.

    File containing descriptive and statistical results for the subset of horses with questionnaire responses collected in conjunction with gait analysis.

    (PDF)

    pone.0308061.s002.pdf (397.8KB, pdf)
    S3 Text. Background questionnaire.

    Pdf file containing the background questionnaire.

    (PDF)

    pone.0308061.s003.pdf (122.6KB, pdf)
    S1 File. Data sets.

    Excel book containing sheets with the data sets used. Sheet ‘Straight-line Hard Surface’, ‘Straight-line Soft Surface’ and ‘Lunge’ contains data from included horses for each condition.

    (XLSX)

    pone.0308061.s004.xlsx (84.5KB, xlsx)
    S2 File. Data set used for statistical analysis.

    Microsoft excel file containing data used in statistical analyses.

    (XLSX)

    pone.0308061.s005.xlsx (27.9KB, xlsx)
    Attachment

    Submitted filename: Response to Reviewers.docx

    pone.0308061.s006.docx (26.7KB, docx)
    Attachment

    Submitted filename: Response to Reviewers.docx

    pone.0308061.s007.docx (23.2KB, docx)

    Data Availability Statement

    All relevant data are within the manuscript and its Supporting Information files


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