Access to this full-text is provided by PLOS.
Content available from PLOS One
This content is subject to copyright.
RESEARCH ARTICLE
Head and pelvic movement asymmetries at
trot in riding horses in training and perceived
as free from lameness by the owner
Marie Rhodin
1
*, Agneta Egenvall
1
, Pia Haubro Andersen
1
, Thilo Pfau
2
1Department of Clinical Sciences, Swedish University of Agricultural Sciences, Uppsala, Sweden,
2Department of Clinical Science and Services, The Royal Veterinary College, University of London,
Hawkshead Lane, North Mymms, Hatfield, United Kingdom
*marie.rhodin@slu.se
Abstract
Recent studies evaluating horses in training and considered free from lameness by their
owners have identified a large proportion of horses with motion asymmetries. However the
prevalence, type and magnitude of asymmetries when trotting in a straight line or on the
lunge have not been investigated. The aim of this study was to objectively investigate the
presence of motion asymmetries in riding horses in training by identifying the side and quan-
tifying the degree and type (impact, pushoff) of forelimb and hind limb asymmetries found
during straight line trot and on the lunge. In a cross-sectional study, vertical head and pelvic
movement symmetry was measured in 222 Warmblood type riding horses, all without per-
ceived performance issues and considered free from lameness by their owners. Body-
mounted uni-axial accelerometers were used and differences between maximum and mini-
mum head (HDmax, HDmin) and pelvic (PDmax, PDmin) vertical displacement between left
and right forelimb and hind limb stances were calculated during straight line trot and on the
lunge. Previously reported symmetry thresholds were used. The thresholds for symmetry
were exceeded in 161 horses for at least one variable while trotting in a straight line, HDmin
(n = 58, mean 14.3 mm, SD 7.1), HDmax (n = 41, mean 12.7 mm, SD 5.5), PDmax (n = 87,
mean 6.5 mm, SD 3.10), PDmin (n = 79, mean 5.7 mm, SD 2.1). Contralateral and ipsilateral
concurrent forelimb and hind limb asymmetries were detected in 41 and 49 horses, respec-
tively. There was a linear association between the straight line PDmin values and the values
on the lunge with the lame limb to the inside of the circle. A large proportion (72.5%) of
horses in training which were perceived as free from lameness by their owner showed
movement asymmetries above previously reported asymmetry thresholds during straight
line trot. It is not known to what extent these asymmetries are related to pain or to mechani-
cal abnormalities. Therefore, one of the most important questions that must be addressed is
how objective asymmetry scores can be translated into pain, orthopedic abnormality, or any
type of unsoundness.
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 1 / 16
a1111111111
a1111111111
a1111111111
a1111111111
a1111111111
OPEN ACCESS
Citation: Rhodin M, Egenvall A, Haubro Andersen
P, Pfau T (2017) Head and pelvic movement
asymmetries at trot in riding horses in training and
perceived as free from lameness by the owner.
PLoS ONE 12(4): e0176253. https://doi.org/
10.1371/journal.pone.0176253
Editor: Juan J Loor, University of Illinois, UNITED
STATES
Received: July 7, 2016
Accepted: April 8, 2017
Published: April 25, 2017
Copyright: ©2017 Rhodin et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: Funded by H1347029, Swedish-
Norwegian Foundation for Equine Research, http://
hastforskning.se/. Marie Rhodin received the
funding. 2014-12003-28225-26, The Swedish
Research Council Formas, http://www.formas.se/.
Marie Rhodin received the funding.
Competing interests: The authors have declared
that no competing interests exist.
Introduction
Orthopedic diseases constitute the most common group of health problems in riding horses
and remain one of the most common causes of interrupting the athletic careers of horses [1,2].
The median length of life for geldings and stallions in Swedish Warmblood horses is 15 years
[3], the age at which many horses can perform at the highest level if they are healthy. The clini-
cal lameness examination has been the prime tool to detect and investigate orthopedic diseases
for decades, but currently applied clinical methods appear rather insensitive to subtle pain and
pathology with resulting small changes in motion symmetry [4–6]. Diseases causing subtle
lameness may hence persist and develop into chronicity before overt clinical signs of lameness
are developed. The weaknesses of visual assessment in horses with mild to moderate lameness
have been described in numerous studies and comprise low inter-rater agreement among cli-
nicians, expectation bias and inaccuracy [4–7]. Therefore early, precise and accurate recogni-
tion of lameness with biomechanical methods has been the focus of research in recent decades.
In trot, the non-lame horse shows a symmetric sinusoidal motion pattern of head and pelvis
which undergoes systematic changes when loading of the limbs changes, for example as a
result of lameness [8–10]. The differences in maximum and minimum position of head or pel-
vis between left/right stances (HDmin, HDmax, PDmin and PDmax) are examples of symme-
try measures commonly used for quantification of lameness and are directly linked to the
underlying changes in limb loading and propulsion [10,11]. Today, commercially available
biomechanical techniques are being developed and validated for detecting changes in gait sym-
metry suitable for research and clinical practice [12–14]. However, only few studies have corre-
lated degree of clinical lameness to the biomechanical results of symmetry measurements. It is
essential to improve our knowledge on how objectively measured asymmetry scores can be
translated into pain, dysfunction, orthopedic abnormalities, or any type of unsoundness.
Many so called “owner-sound” horses, free from lameness according to the judgement of
their owner, that are in regular training and competition show asymmetric motion patterns to
a similar degree as horses examined and treated for orthopedic pathology. Two studies, objec-
tively evaluating the motion pattern of 201 and 23 riding horses in training and judged as
sound by their owners, showed that 107 (53%) and 14 (61%) horses, respectively, had asym-
metric head and/or pelvic movements measured during straight line trot [15,16]. In two stud-
ies [17,18] 506 and 57 “owner-sound” horses were evaluated by visual assessment of the
motion pattern under different circumstances (in straight line trot, lungeing and when ridden)
and 46% and 65% horses respectively showed abnormal movements interpreted as pathologi-
cal conditions. Landman et al. [19] found that 19.5% of 399 horses examined before purchase
showed a lameness of degree two or more on a 0–5 scale. None of these studies quantified the
distribution of forelimb or hind limb lameness, the degree of asymmetry or how the asymmet-
ric motion pattern was affected by circular motion, i.e. when trotting on the lunge, a com-
monly employed exercise during lameness and pre-purchase examinations. It is not known
whether these asymmetries are influenced by horse age, horse size, equestrian discipline or the
horse’s performance level. Murray et al. [20] investigated the association of type of sport and
performance level with specific orthopedic conditions and found that show jumping horses
were at increased risk of forelimb deep digital flexor tendinitis whereas dressage horses were at
significantly increased risk of hind limb suspensory ligament injury. Whether these differences
between disciplines may also be reflected by differences in motion symmetry among horses in
training has never been investigated.
A recent study of 60 performing polo ponies revealed that 60–67% showed gait asymmetries
which were not related to age or preferentially left or right sided [21] but the clinical relevance
of these asymmetries are still unknown.
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 2 / 16
Most studies on lameness have been performed in horses trotting on the straight. However
lungeing is commonly used during lameness and pre-purchase evaluations since it induces dif-
ferences in the severity of apparent lameness compared to trot on the straight [22]. Lungeing
also affects the symmetry of the motion pattern in sound horses [23,24] and this circle-depen-
dent asymmetry will be superimposed on the pre-existing lameness of the horse making it
more, or less, visible [23]. Whether this circle-dependent asymmetry will increase or decrease
the degree of asymmetry depends on whether the limb contributing to the asymmetry is on
the inside or outside of the circle [23]. This phenomenon is very relevant for diagnostic proce-
dures in clinical cases but has not yet been investigated thoroughly.
The degree of lameness varies between strides but how this inter-stride variability changes
with increased degree of lameness is not well described and may be important knowledge
when evaluating lame horses [25]. It is also not described for different lameness scales whether
the scoring should be based on the lamest stride or an average of all strides during a trot up or
which strides should be used for comparison before and after diagnostic analgesia [26].
The aim of this study was to objectively investigate prevalence and nature of motion asym-
metries in riding horses in training, perceived as being free from lameness by their rider, by
identifying the side and quantifying the degree and type (impact, pushoff) of forelimb and
hind limb asymmetries during trot on the straight and on the lunge, using a commercial sen-
sor-based system for lameness detection. We hypothesised that the effect of lungeing would
neutralise the asymmetry seen on straight line trot in one lungeing direction and exacerbate
the asymmetry in the opposite direction. We also hypothesized that stride variability during a
test run decreases with increased degree of asymmetry and therefore the association between
proportion of left /right asymmetric strides and degree of asymmetry was investigated. Finally,
we wanted to investigate if discipline, performance level, age, gender and size of the horse were
related to the prevalence of gait asymmetry.
Material and methods
This study has been approved by the Ethical Committee for Animal Experiments, Uppsala,
Sweden (permission number C251/9, C48/13) and informed consent for data collection was
obtained from the horse owners prior to the study.
Study design
Cross-sectional study of movement symmetry in riding horses in training.
Horses
Invitations, containing an informed consent form, to participate in the study were extended to
horse owners based on convenience sampling between 2009 and 2014. Inclusion criteria:
Horses (>148 cm height) perceived to be free from lameness by their owner/rider (interview)
and ridden regularly, at least 2–3 times per week. Exclusion criteria were reports of lameness,
health problems or medical treatments within the last 6 months or horses not cooperating
when ridden or on the lunge. Gender, age, breed, height, discipline and level of performance
were recorded for each horse according to information given by the owner. There were 81
mares, 3 stallions and 138 geldings with an age distribution of 3–25 years (median 10 years)
and a withers height of 150–182 cm (median 165 cm). The horses belonged to 122 different
owners (range 1–58 horses/owner, median 1 horse/owner). The three owners with the highest
number of horses (58, 10 and 8 horses) were teaching facilities where the horses were ridden
by different riders. Of the 222 horses, there were 219 Warmblood type horses and 3 cross-
breeds of unknown breed.
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 3 / 16
Data collection protocol
Motion analysis of the horses in trot, when handled by the owner, was performed in three trials
in random order: in a straight (S) line on a hard surface (concrete or gravel based); during lun-
geing on a soft surface, (sand or fibre based) to the left (L); and during lungeing to the right
(R). Circle diameters varied between 10–15 m, using similar diameters within horse for the left
and right reins.
Motion analysis
A commercial inertial measure unit (IMU) based gait analysis system (Lameness Locator,
Equinosis, St. Louis, MO, USA) for lameness detection was used [14]. Briefly, one uni-axial
accelerometer was mounted to a head bumper attached to the bridle over the poll and one uni-
axial accelerometer was taped to the midline of the pelvis at the level of the tubera sacrale.
Finally, one uni-axial gyroscope was attached dorsally to the proximal and middle phalanges
of the right forelimb. Vertical uni-axial acceleration was recorded at 200 Hz with 8 bit digital
resolution and data were transmitted wirelessly from the sensors to a nearby laptop computer
running the data collection software.
Data processing
Data from all straight line and lungeing trials were processed with the software package for the
gait analysis system. Raw uni-axial acceleration signals from head and pelvis sensors, aligned
with the global vertical axis in the standing position, were first transformed into displacement
signals using a custom-designed, error-correcting, double-integration technique and the signal
from the right forelimb gyroscope was used for stride splitting [14]. From the displacement
signal local maxima and minima were identified (two per stride). Differences in minimum
head (HDmin) and pelvis (PDmin) height during left and right stance phases and differences
in maximum head (HDmax) and pelvis (PDmax) height after left and right stance phases were
computed for each stride (Fig 1).
Asymmetric head movement is attributed to forelimb asymmetry and asymmetric pelvis
motion is attributed to hind limb asymmetry. Here, a horse presenting with reduced head
movement during left front stance is referred to as left front asymmetric, a horse presenting
with reduced pelvic movement during left hind stance as left hind asymmetric [9]. Removal of
Fig 1. Example of vertical head movement in a horse with right forelimb lameness resulting in
positive HDmin and HDmax values. Approximate timing of left (L) and right (R) forelimb stance is indicated
by grey bars. Pelvic movement symmetry is calculated in the same way from vertical pelvis movement signal.
https://doi.org/10.1371/journal.pone.0176253.g001
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 4 / 16
single outliers for the head movement was performed in the software package. The mean
amplitude and sign of HDmin, HDmax, PDmin, and PDmax for all strides in a trial were cal-
culated from the signal, resulting in either a positive or negative mean value for each variable
and trial. Positive values indicated asymmetries attributed to the right and negative values
asymmetries attributed to the left forelimb or hind limb HDmin
right/left
, HDmax
right/left
,
PDmin
right/left
, and PDmax
right/left
. [9]. The number of left and right asymmetric strides
according to the sign of HDmin and PDmin respectively were also calculated for each trial.
Criteria for motion asymmetry developed by Keegan et al. [14] were applied to absolute
mean differences, over all strides in each horse’s straight line trial(s). Gait parameters of
straight line and lungeing trials were retained for further analysis for horses with straight line
values larger than 6 mm for the head movement (HDmin or HDmax) and 3 mm for the hind
quarter (pelvic) motion (PDmin or PDmax) and with standard deviations less than their
respective means.
For the horses with mean HDmax and/or HDmin values outside the thresholds the vector
sum (VS) of the mean HDmax and HDmin was calculated as ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
HDmax2þHDmin2
pand
assigned to the left or right side (VS
left
and VS
right
) depending on whether HDmin was positive
or negative [9].
Statistical methods
Descriptive statistics were calculated. To identify any relationships between motion asymmetry
on the straight and on the lunge, the values for HDmin, HDmax, PDmin and PDmax during
straight-line trot were plotted (on the x-axis, for visual evidence of linearity) and regressed
against HDmin, HDmax, PDmin and PDmax values during lungeing (y-axis). This procedure
was implemented three times: 1) for trials with the asymmetric limb to the inside of the circle,
2) with the asymmetric limb to the outside of the circle and also against 3) the sum of the
excursion values from both lungeing directions. Likewise the HDmin and PDmin values dur-
ing straight line trot were regressed against the proportion of right forelimb and right hind
limb asymmetric strides, respectively, to identify any relationship between the degree of move-
ment asymmetry on the straight (only straight) and the proportion of left/right asymmetric
strides.
Mixed model analysis (SAS Institute Inc. (2014) SAS/STAT 13.2 User’s Guide, SAS Institute
Inc, Cary, North Carolina) was performed for the analyses with respect to gender, age, height
and discipline, all included as fixed effects, and absolute values of the outcome variables
(HDmin, HDmax, PDmin and PDmax) were used. These outcome variables were not nor-
mally distributed. Box-Cox transformation along Tukeys ladder of powers was performed and
used to select the best transformation closest to normality. Each of the independent variables
was tried as a fixed effect one at a time, while controlling for direction as a fixed effect. The for-
mat of the tested variables was as follows: male horses (geldings and stallions) were compared
with mares; main discipline of the horses was divided into general (including 5 event horses),
show-jumping or dressage. Further, height at the withers was divided into four categories
[<155 cm, 155<164 cm, 164<172 cm and >172 cm] and age into 4 categories [<6 years,
6<11 years, 11<16 years and >16 years]. These dummy variables suggested that height at
withers and age were reasonably linear when modelled against the outcomes and were there-
fore modelled as linear. Random effect was horse within owner. The covariance structure was
variance component. Models are shown if group p-values <0.05 (type III) and at least one
pairwise comparison p <0.05. A description of the variables used and the data is available in
supporting information (S1 Data).
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 5 / 16
Results
Study population
Of the 222 horses, 161 (72.5%) Warmblood type horses had absolute values outside thresholds
for straight line trot for at least one symmetry variable (HDmin (n = 58, mean 14.3, median
11.8, range 6.6–35.2 mm), HDmax (n = 41, mean 12.7, median 11.1, range 6.4–35.3 mm),
PDmin (n = 79, mean 5.6, median 5.1, range 3.1–12.3 mm) and PDmax (n = 87, mean 6.5,
median 5.4, range 3.1–15.4 mm). These horses were retained for further analysis and the
horses with symmetrical movement on the straight were excluded.
Of the 161 horses, 57 were mares, 3 were stallions and 101 were geldings with an age distri-
bution of 3–25 years (median 11 years), withers height 150–182 cm (median 165 cm, data on
height was missing in 19 horses) and the horses belonged to 74 different owners (range 1–44
horses/owner, median 1 horse/owner).
For straight line trot there were (mean ±SD), 30 ±12.3 strides evaluated per trial. For lunge-
ing to the left and right 47 ±16.7 respectively 49 ±17.4 strides were evaluated per trial. Contra-
lateral and ipsilateral concurrent forelimb and hind limb asymmetries on the straight were
detected in 41 and 49 horses, respectively.
Effect of lungeing direction
Mean HDmin
right
, HDmin
left
, HDmax
right
, HDmax
left
, VS
right
, VS
left
, PDmin
right
, PDmin
left
,
PDmax
right
and PDmax
left
values for all horses exceeding the thresholds for straight line trot
and their values on the lunge are shown in Table 1.
Effect of age, level, discipline, gender and withers height
Outcome variables (absolute values of asymmetry variables) were modelled raised to the
power of 0.25. PDmin was significantly (p = 0.01) higher for dressage horses (n = 65) (back-
transformed value 5.3 mm) compared to show jumping horses (n = 33) (3.8 mm). In addition,
controlling for direction, PDmin was also significantly (p = 0.001) higher on the left (5.9 mm)
or right (5.9 mm) reins compared to straight line (2.7 mm) measurements.
PDmax was significantly higher (p = 0.01) for horses of advanced level (n = 12) (5.0 mm)
compared to horses of intermediate level (n = 52) (3.1 mm). Models with a group p-value <0.05
are presented (S1 Table).
After controlling for owner, HDmin and HDmax were not affected by age, level, discipline,
gender or withers height.
Inter-stride variability
Scatter plots and regression lines/equations between the HDmin and PDmin values at straight
line and the proportion of left or right limb asymmetric strides for all 161 horses are shown in
Fig 2. Linear relationships between the mean value of HDmin and PDmin and the proportion
of lame strides are demonstrated.
Straight line asymmetries compared to asymmetries on the lunge
Figs 3–6present scatter plots and regression lines/equations for the 161 horses. Comparisons
were made for HDmin, HDmax, PDmin, PDmax values between straight line measurements
and measurements on the lunge with the asymmetric limb to the inside (Inner) or outside
(Outer) of the circle, or the sum (Sum) of the values from both lungeing directions. All regres-
sion lines showed a positive association between straight line values and either Inner, Outer or
Sum except for the straight line PDmin values and the association to the Outer PDmin values,
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 6 / 16
when the asymmetric limb was to the outside of the circle (Fig 5). All associations were signifi-
cant except for the association between straight line HDmax and PDmax values to the values
of the sum of both lungeing directions (Figs 4and 6).
Discussion
Degree of asymmetries
In the present study, a remarkably high number of horses (72.5%) in training, judged as being
free from lameness by their owner, show motion asymmetries. This raises the question
whether these asymmetries are caused by pain and/or pathology or could simply be a biologi-
cal variation.
Table 1. Forelimb (HDmin, HDmax and VS) and hind limb (PDmin and PDmax) asymmetries, are presented for the horses (n) exceeding the thresh-
old value for symmetry for straight line motion and their corresponding values for the left and right lungeing direction. Positive values are attributed
to a right limb and negative values a left limb asymmetry.
Percentiles
Variable n Mean Std 5th 25th 50th 75th 95th
Straight
HDmin
right
29 12.8 6.4 7.2 8.7 11.1 15.2 23.9
HDmin
left
29 -15.8 7.5 -30.5 -20.2 -13.5 -10.0 -7.9
HDmax
right
24 11.3 3.6 7.4 8.5 10.7 13.5 17.4
HDmax
left
17 -14.6 7.2 -35.3 -17.4 -13.5 -9.3 -6.4
VSleft 40 17.4 8.3 9.0 11.8 15.5 20.9 35.0
Vsright 40 14.1 5.9 7.2 9.7 13.0 16.0 24.7
PDmin
right
36 5.8 2.3 3.5 4.2 5.0 7.2 11.1
PDmin
left
43 -5.5 1.8 -8.7 -6.1 -5.2 -3.9 -3.4
PDmax
right
43 6.9 3.4 3.5 4.1 5.4 9.6 13.6
PDmax
left
44 -6.1 2.8 -12.5 -6.6 -5.3 -4.3 -3.7
Left circle
HDmin
right
29 11.0 12.6 -3.7 1.5 9.7 15.4 34.8
HDmin
left
29 -7.6 14.2 -35.5 -14.0 -10.4 -4.4 17.4
HDmax
right
24 4.0 9.0 -8.9 -2.7 4.0 10.0 20.7
HDmax
left
17 -3.6 11.3 -26.4 -12.1 -5.3 5.6 14.8
VSleft 40 15.9 9.9 3.7 10.3 12.8 20.1 36.9
VSright 40 16.0 10.7 2.6 9.3 13.9 20.5 38.9
PDmin
right
36 -2.1 6.1 -11.7 -5.9 -1.0 0.8 5.1
PDmin
left
43 -12.9 8.1 -24.2 -16.3 -12.7 -6.5 -3.7
PDmax
right
43 5.9 6.3 -6.0 2.3 5.3 9.7 16.9
PDmax
left
44 -1.9 4.0 -7.7 -4.1 -2.5 -0.1 4.9
Right circle
HDmin
right
29 2.1 14.4 -26.7 -6.5 14.0 10.5 25.2
HDmin
left
29 -15.1 15.6 -40.7 -27.0 -12.0 -2.9 6.2
HDmax
right
24 10.1 9.5 -4.1 3.2 8.9 18.0 24.7
HDmax
left
17 -8.3 13.3 -35.5 -16.4 -4.8 -0.5 15.1
VSleft 40 21.1 14.0 3.1 10.2 18.8 27.3 52.0
VSright 40 16.2 11.6 4.7 7.9 12.8 19.0 37.5
PDmin
right
36 12.5 6.9 -0.5 9.1 14.0 16.5 22.7
PDmin
left
43 3.1 6.6 -4.8 -1.2 3.3 7.3 10.4
PDmax
right
43 2.7 4.8 -4.6 -0.1 1.9 5.4 11.4
PDmax
left
44 -7.0 4.9 -16.9 -9.7 -6.8 -3.6 -0.5
https://doi.org/10.1371/journal.pone.0176253.t001
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 7 / 16
In a previous study of ten horses with induced forelimb lameness [23], the mean degree of
asymmetry for HDmin
left/right
was -26.1/20.1 mm. The 5
th
and 95
th
percentiles of the present
study exceed these values, presented in Table 1, but the mean values were lower (HDmin
left/right
-15.8/12.8 mm). Further, the 10 horses with induced lameness showed HDmax
left/right
values
(-15.3/14.3 mm) of a similar degree to or slightly higher than the mean values of HDmax
left/right
(-14.6/11.3 mm) for the horses in the present study. Maliye et al., [27,28] investigated 28 and 37
horses with naturally occurring forelimb and hind limb lameness respectively, evaluated both
visually and objectively with the same system as in the present study, and obtained mean values
of 18.3 mm (inter quartile range 12.2–32.0) for the VS (of HDmin and HDmax), compared to
16.8 mm in the present study for the forelimb asymmetric horses. For the clinically hind limb
lame horses, the absolute mean PDmax was 5.10 mm (inter quartile range 2.95 to 8.77) com-
pared to 6.9 mm for right limb and 6.1 mm for left asymmetric horses in the present study.
These comparisons show that many horses, free from lameness according to their owners, pres-
ent with objectively measured lameness parameters of the same magnitude or larger than horses
thought to have clinically important lameness.
For the horses with induced hind limb lameness [23] the mean PDmin
left/right
values were
-9.0/6.2 mm and this degree is in accordance with six clinically hind limb lame horses investi-
gated by Maliye et al., [28] with a group-mean value for PDmin of 6.0 mm (absolute value).
The mean values for PDmin
left/right
(-5.5/5.8 mm) were slightly lower in the present study but
the 25
th
percentile (-8.7) and 75
th
percentile (7.2) exceeded these values. Thus, the results of
the present study compared to similar results of previous studies of lameness in clinically lame
horses using the same measuring system, indicate that there is considerable overlap between
Fig 2. Scatter plot and regression analysis between mean values of differences in minimum head
(HDmin) and pelvis (PDmin) position and the proportion of left/right limb asymmetric strides at
straight-line trot for each trial. The p-values shown in the regression equations refers to the slopes
(n = 161).
https://doi.org/10.1371/journal.pone.0176253.g002
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 8 / 16
clinically lame horses and horses in training perceived as free from lameness according to their
owner. For many horses in the current study, this means that, were they presented to a veteri-
narian with a complaint of poor performance or lameness (for whatever reason), the veterinar-
ian would likely conduct a full lameness examination.
Asymmetries are generally caused by differences in loading and force production between
limbs [11,29]. However, we do not know whether such asymmetries always are related to pain.
This also means, that there is a limited understanding of to what extent asymmetries are
related to an underlying disease process and whether their presence always poses a welfare
issue. Only full clinical lameness examinations with diagnostic analgesia or analgesic testing by
systemically administered analgesic drugs could possibly answer this question. Longitudinal
studies on motion asymmetry and incidences of different orthopedic disorders are needed to
answer this and other significant questions, as for example whether the higher pelvic motion
asymmetries (PDmin) observed in the dressage horses in the present study indeed are related
to an increased risk for developing hind limb suspensory ligament injuries that has been
described by Murray et al. [20].
It may be speculated why owners and riders do not notice these asymmetries or which fac-
tors influence the decision of referring their horse to a veterinarian. One reason for not notic-
ing that the horse moves asymmetrically could be that the horse is ridden on a soft surface,
while asymmetry was measured on a hard surface, where disease processes might get provoked
by increased forces, resulting in increased pain [16]. A common reason for referring a horse
Fig 3. Scatter plot and regression analysis between straight line HDmin (mean values of differences
in minimum head position) values (x-axis) and values from measurements on the lunge (y-axis) with
the asymmetric limb to the inside (Inner) or outside (Outer) of the circle, or the sum (Sum) of the
values from both lungeing directions for all horses (n = 161). The p-values shown refer to the slopes of
the regression equations.
https://doi.org/10.1371/journal.pone.0176253.g003
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 9 / 16
for a lameness examination is not only lameness, but also reduced performance or resistant
behaviour of the horse when ridden, perhaps occurring with increasing frequency [22]. It may
therefore also be possible that there was a difference in temperament between the horses inves-
tigated in the present study and horses examined for lameness.
Also, the riding skills and style of the rider may influence the symmetry of head and pelvic
motion of the horse during riding and thus contribute to masking of forelimb asymmetry [29]
or hind limb lameness during rising trot [30,31]. Riders or trainers may also interpret persistent
movement asymmetries as laterality rather than signs of pain. We have no information about
whether the horse’s movement had been evaluated regularly by rider, trainer or veterinarian.
Based on our results, we recommend that the movement of horses is inspected regularly to facili-
tate detection of asymmetries at an early stage. Further studies need to be conducted to see
whether these are linked to orthopedic problems. One recent study suggested that visual assess-
ment of “saddle slip” i.e. saddle movement to one side during ridden exercise, could be a sign of
hind limb lameness in ridden horses [17] that could be more readily detected by the rider or the
trainer than a small asymmetric pelvic motion. Further studies are needed to verify this state-
ment. The availability of smartphones and sensors that can measure and interpret acceleration
data from horse movement suggests that owners may soon be able to track their horse’s move-
ment through time, which opens up new possibilities for early lameness detection [32]. Adequate
methods of training horse owners to undertake this task with the necessary repeatability and to
develop automated methods for assessing data quality should be investigated. The emergence of
Fig 4. Scatter plot and regression analysis between straight line HDmax (mean values of differences
in maximum head position) values (x-axis) and values from measurements on the lunge (y-axis) with
the asymmetric limb to the inside (Inner) or outside (Outer) of the circle, or the sum (Sum) of the
values from both lungeing directions for all horses (n = 161). The p-values shown refer to the slopes of
the regression equations.
https://doi.org/10.1371/journal.pone.0176253.g004
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 10 / 16
these technologies warrants the continued investigation of the biological meaning of movement
asymmetries.
Lungeing
The strong effects of lungeing on the symmetry of the horses in this study confirms that
circle dependent effects influence motion symmetry in both horses free from lameness and
horses with induced lameness [15,23]. In the present study when lunged on a soft surface,
horses with PDmin values outside normal limits on the straight line showed increased
asymmetry when the asymmetric limb was on the inside of the circle and decreased asym-
metry when the limb was on the outside of the circle (Table 1). The opposite was seen for
PDmax asymmetries. Horses with HDmin values outside normal limits were more asym-
metric with the asymmetric limb on the outside of the circle and showed more symmetri-
cal movement with the asymmetric limb on the inside of the circle. The circle-dependent
findings for head movement were less consistent than for pelvic motion and some horses
switched the side of the asymmetry (Table 1) during lungeing compared to straight line
measurement, showing bilateral asymmetries.
Since circular movement induces asymmetries, especially in the pelvis (PDmin), the initial
asymmetry observed on the straight may be masked with the asymmetric limb on the outside
of the circle (Fig 5). Therefore when evaluating horses on the lunge, both an increase or a
decrease in symmetry could be a sign of positive diagnostic analgesia or of effective treatment
Fig 5. Scatter plot and regression analysis between straight line PDmin (mean values of differences in
minimum pelvic position) values (x-axis) and values from measurements on the lunge (y-axis) with
the asymmetric limb to the inside (Inner) or outside (Outer) of the circle, or the sum (Sum) of the
values from both lungeing directions for all horses (n = 161). The p-values shown refer to the slopes of
the regression equations.
https://doi.org/10.1371/journal.pone.0176253.g005
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 11 / 16
depending on the lame limb being on the inside or the outside of the circle. The high correla-
tion between straight line asymmetries and the sum of both lungeing directions indicates that
the asymmetries generally are amplified by the circle dependent asymmetries in one direction
and attenuated when changing direction. This is also in accordance with empiric clinical expe-
rience. We believe that lungeing simply increases the degree of asymmetry from being difficult
or impossible to detect by eye to more clearly exceeding the previously investigated limits for
human visual perception [33]. The benefits of lungeing may hence be more unclear, if the
lameness is readily visible (or at least measurable) on the straight line. Lungeing might increase
the accuracy of detecting the primary lame limb but could also decrease the accuracy due to
the low inter-rater agreement when assessing lameness on the lunge [4]. In clinical text books,
descriptions of increased lameness for certain orthopedic disorders are given when the affected
limb is on the outside (proximal suspensory desmitis, medial carpal problems, medial sesa-
moid bone problems) or on the inside (bilateral forelimb lameness) of the circle [22]. Quanti-
tative assessment may provide essential evidence for validating these observations through
application of diagnostic analgesia to localize the origin of pain within the affected limb. Such
important methodological questions can be answered by biomechanical studies of large popu-
lations of well documented clinical cases, before and after diagnostic analgesia. In the present
study 49 horses showed ipsilateral and 41 horses showed contralateral concurrent forelimb
and hind limb asymmetries and we do not know if these asymmetry patterns reflect single or
multi limb lameness. There may also be differences in terms of the measured asymmetries
Fig 6. Scatter plot and regression analysis between straight line PDmax (mean values of differences
in maximum head position) values (x-axis) and values from measurements on the lunge (y-axis) with
the asymmetric limb to the inside (Inner) or outside (Outer) of the circle, or the sum (Sum) of the
values from both lungeing directions for all horses (n = 161). The p-values shown refer to the slopes of
the regression equations.
https://doi.org/10.1371/journal.pone.0176253.g006
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 12 / 16
during circular movement with different effects on primary and compensatory movement
asymmetry. This needs further investigation ideally in horses with diagnosed orthopedic defi-
cits assessed before and after diagnostic analgesia on the straight line and on the lunge.
Inter-stride variability
In the present study, the high correlation between the proportion of left or right limb asymme-
tries and the increasing value of HDmin and PDmin (Fig 2) raises important questions when
evaluating horses with subtle lameness. For horses with subtle asymmetries, the asymmetries
may appear intermittently and would thus not be visible or measurable in every stride. There-
fore, both the proportion of lame strides and the magnitude of the asymmetries must be taken
into account when evaluating lameness for example before and after diagnostic analgesia. The
high inter-stride variability in less asymmetric horses shown here may also contribute to the
well documented low inter-rater agreement among veterinarians evaluating subtle lameness.
High inter-stride variability may also explain how easily expectation bias can influence the
visual assessment when ‘hoping for’ either lame or sound strides after a block or treatment [6].
Peham et al. [25] showed that inter-stride variability of stride length decreased with increasing
lameness but the number of left or right lame strides was not studied. It could be possible that
high inter-stride variability is a sign of a non-lame horse. A pain free horse may ‘not care’ how
it moves in each stride and hence some strides may be more symmetrical than others. In con-
trast to this, a lame horse in pain could have developed a preferred way of moving that mini-
mises pain, and as a consequence reduces inter-stride variability.
In this study, proportions of left/right asymmetries were close to 50/50%. Therefore, rea-
sons such as rider handedness, or horse laterality or the fact that horses are often handled from
the left side are unlikely explanations of the results.
Limitations of the study
No clinical examination was performed on the horses and the underlying causes of the motion
asymmetries are not known. The present study used a convenience sample of horses, stabled
within reasonable proximity to the authors. It is possible that some owners offered their horse
(s) for participation in the study because they suspected some locomotor problems in their
horses, resulting in some ‘inclusion’ bias. However, all horses had been in training for at least 6
months previous to the study without referral to a veterinarian. Some other relations between
motion symmetry, performance level, age, withers height and discipline may not have been
detected due to a small sample size.
Conclusions
A major proportion of horses in regular training show motion asymmetries of similar magni-
tude to asymmetries found in horses examined and treated for lameness. It is not known to
what extent these asymmetries are caused by pain and hence may present a potential welfare
problem or may be related to poor performance. Further studies are needed to investigate this.
It may be a welfare problem, if indeed a proportion of such asymmetries were not painful but
caused by inherent natural laterality or by poor/asymmetric training. Increased knowledge
about the relationship between pain and movement asymmetry is needed to avoid excessive
lameness investigations and unnecessary treatment or euthanasia. One of the most important
questions to be addressed before biomechanical objective asymmetry scores can be translated
into pathology, is to which extent pain, dysfunction or orthopedic abnormality and motion
asymmetry are synonymous conditions. The high inter-stride variability seen in horses pre-
senting mild movement asymmetries may contribute to the well documented low inter-rater
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 13 / 16
agreement among veterinarians evaluating subtle lameness and may also explain how expecta-
tion bias can influence visual assessment when expecting either lame or sound strides after a
diagnostic block or treatment. To further understand any causal relationship between disci-
plines, performance level and motion symmetry longitudinal studies are needed.
Supporting information
S1 Table. Least square means of univariable fixed effects from mixed models. Univariable
fixed effects with owner as a random effect for two dependent variables (PDmin and PDmax)
for variables with group-level p-values <0.05. BT- back-transformed estimate and standard
error (SE). NS- non significant pairwise comparison.
(XLSX)
S1 Data. Data set used for the data analysis. Excel sheet containing description of variables
used for the analysis.
Sheet ‘reduced_content_rowsred’ contains descriptions of the data and explanations of what
the variable names mean. Sheet ‘data_rowsred’ contains the data.
(XLSX)
Author Contributions
Conceptualization: MR TP AE PHA.
Data curation: MR TP AE PHA.
Formal analysis: MR TP AE.
Funding acquisition: MR TP AE PHA.
Investigation: MR TP AE.
Methodology: MR TP AE PHA.
Project administration: MR TP.
Resources: MR TP.
Software: AE.
Supervision: MR PHA.
Validation: MR TP AE PHA.
Visualization: MR TP AE PHA.
Writing – original draft: MR TP AE PHA.
Writing – review & editing: MR TP AE PHA.
References
1. Egenvall A, Penell JC, Bonnett BN, Olson P, Pringle J. Mortality of Swedish horses with complete life
insurance between 1997 and 2000: variations with sex, age, breed and diagnosis. Vet Rec. 2006;
158:397–406. PMID: 16565338
2. Penell JC, Egenvall A, Bonnett BN, Olson P, Pringle J. Specific causes of morbidity among Swedish
horses insured for veterinary care between 1997 and 2000. Vet Rec. 2005; 157:470–7. PMID:
16227382
3. Wallin L. Livsla
¨ngd och utslagsorsaker hos ha
¨st. http://stud.epsilon.slu.se/4095/. 2012
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 14 / 16
4. Hammarberg M, Egenvall A, Pfau T, Rhodin M. Rater agreement of visual lameness assessment in
horses during lungeing. Equine Vet J. 2016; 48(1):78–82. https://doi.org/10.1111/evj.12385 PMID:
25399722
5. Keegan KG, Dent EV, Wilson DA, Janicek J, Kramer J, Lacarrubba A, et al. Repeatability of subjective
evaluation of lameness in horses. Equine Vet J. 2010; 42:92–7. https://doi.org/10.2746/
042516409X479568 PMID: 20156242
6. Arkell M, Archer RM, Guitian FJ, May SA. Papers & Articles Evidence of bias affecting the interpretation
of the results of local anaesthetic nerve blocks when assessing lameness in horses. Vet Rec.2006;
159:346–349. PMID: 16963714
7. Hewetson M, Christley RM, Hunt ID, Voute LC. Investigations of the reliability of observational gait anal-
ysis for the assessment of lameness in horses. Vet Rec. 2006; 158:852–7. PMID: 16798953
8. Rhodin M, Pfau T, Roepstorff L, Egenvall A. Effect of lungeing on head and pelvic movement asymme-
try in horses with induced lameness. Vet J. 2013; 198 Suppl:e39–45. https://doi.org/10.1016/j.tvjl.2013.
09.031 PMID: 24140227
9. Buchner HH, Savelberg HH, Schamhardt HC, Barneveld A. Head and trunk movement adaptations in
horses with experimentally induced fore- or hindlimb lameness. Equine Vet J. 1996;28(1):71–6. PMID:
8565958
10. McCracken MJ, Kramer J, Keegan KG, Lopes M, Wilson DA, Reed SK, et al. Comparison of an inertial
sensor system of lameness quantification with subjective lameness evaluation. Equine Vet J. 2012; 44
(6):652–6. https://doi.org/10.1111/j.2042-3306.2012.00571.x PMID: 22563674
11. Bell RP, Reed SK, Schoonover MJ, Whitfield CT, Yonezawa Y, Maki H, et al. Associations of force plate
and body-mounted inertial sensor measurements for identification of hind limb lameness in horses. Am
J Vet Res. 2016; 77(4):337–45. https://doi.org/10.2460/ajvr.77.4.337 PMID: 27027831
12. Warner SM, Koch TO, Pfau T. Inertial sensors for assessment of back movement in horses during loco-
motion over ground. Equine Vet J. 2010; 42 (Suppl. 38):417–24.
13. Pfau T, Witte TH, Wilson AM. A method for deriving displacement data during cyclical movement using
an inertial sensor. J Exp Biol. 2005; 208 (Pt 13):2503–14. https://doi.org/10.1242/jeb.01658 PMID:
15961737
14. Keegan KG, Kramer J, Yonezawa Y, Maki H, Frank Pai P, Dent EV, et al. Assessment of repeatability
of a wireless, inertial sensor-based lameness evaluation system for horses. Am J Vet Res. 2011; 72
(9):1156–63. https://doi.org/10.2460/ajvr.72.9.1156 PMID: 21879972
15. Rhodin M, Roepstorff L, French A, Keegan KG, Pfau T, Egenvall A. Head and pelvic movement asym-
metry during lungeing in horses with symmetrical movement on the straight. Equine Vet J. 2015;
48:315–20. https://doi.org/10.1111/evj.12446 PMID: 25808700
16. Pfau T, Jennings C, Mitchell H, Olsen E, Walker A, Egenvall A, et al. Lungeing on hard and soft sur-
faces: Movement symmetry of trotting horses considered sound by their owners. Equine Vet J. 2015; 48
(1):83–9
17. Greve L, Dyson SJ. The interrelationship of lameness, saddle slip and back shape in the general sports
horse population. Equine Vet J. 2014; 46(6):687–94. https://doi.org/10.1111/evj.12222 PMID:
24372949
18. Dyson SJ, Greve L. Subjective Gait Assessment of 57 Sports Horses in Normal Work: A Comparison of
the Response to Flexion Tests, Movement in Hand, on the Lunge, and Ridden. Journal of Equine Vet
Science. 2016; 38; 1–7
19. Landman MAAM, de Blaauw JA, van Weeren PR, Hofland LJ. Field study of the prevalence of lameness
in horses with back problems. Vet Rec. 2004; 155(6):165–8. PMID: 15357376
20. Murray RC, Dyson SJ, Tranquille C, Adams V. Association of type of sport and performance level with
anatomical site of orthopaedic injury diagnosis. Equine Vet J. 2006; 38 (Suppl.36):411–6.
21. Pfau T, Parkes RS, Burden ER, Bell N, Fairhurst H, Witte TH. Movement asymmetry in working polo
horses. Equine Vet J. 2016; 48(4):517–22. https://doi.org/10.1111/evj.12467 PMID: 26037947
22. Baxter, GM ST. Lameness in Horses. In: Gary M. Baxter, editor. Sixth. Chichester, West Sussex,
England: Wiley-Blackwell; 2011. p. 115 and 479.
23. Rhodin M, Pfau T, Roepstorff L, Egenvall A. Effect of lungeing on head and pelvic movement asymme-
try in horses with induced lameness. Vet J. 2013; 198: e39–45 https://doi.org/10.1016/j.tvjl.2013.09.031
PMID: 24140227
24. Pfau T, Stubbs NC, Kaiser LJ, Brown LEA, Clayton HM. Effect of trotting speed and circle radius on
movement symmetry in horses during lunging on a soft surface. Am J Vet Res. 2012; 73(12):1890–9.
https://doi.org/10.2460/ajvr.73.12.1890 PMID: 23176414
25. Peham C, Licka T, Girtler D, Scheidl M. The Influence of Lameness on Equine Stride Length Consis-
tency. Vet J. 2001; 162:153–7. https://doi.org/10.1053/tvjl.2001.0593 PMID: 11531399
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 15 / 16
26. Dyson S. Can lameness be graded reliably? Equine Vet J. 2011; 43(4):379–82. https://doi.org/10.1111/
j.2042-3306.2011.00391.x PMID: 21631579
27. Maliye S, Voute LC, Marshall JF. Naturally-occurring forelimb lameness in the horse results in signifi-
cant compensatory load redistribution during trotting. Vet J. 2015; 204(2):208–13. https://doi.org/10.
1016/j.tvjl.2015.03.005 PMID: 25862395
28. Maliye S, Marshall JF. Objective assessment of the compensatory effect of clinical hind limb lameness
in horses: 37 cases (2011–2014). J Am Vet Med Assoc. 2016; 249(8):940–4. https://doi.org/10.2460/
javma.249.8.940 PMID: 27700267
29. Licka T, Kapaun M, Peham C. Influence of rider on lameness in trotting horses. Equine Vet J. 2004;
36:734–6. PMID: 15656506
30. Robartes H, Fairhurst H, Pfau T. Head and pelvic movement symmetry in horses during circular motion
and in rising trot. Vet J. 2013; 198 Suppl:e52–8. https://doi.org/10.1016/j.tvjl.2013.09.033 PMID:
24144771
31. Roepstorff L, Egenvall A., Rhodin M, Bystro
¨m A., Johnston C, Weeren PR, et al. Kinetics and kinemat-
ics of the horse comparing left and right rising trot. Equine Vet J. 2009 5; 41(3):292–6. PMID: 19469238
32. Pfau T, Weller R. Comparison of a standalone consumer grade smartphone with a specialist inertial
measurement unit for quantification of movement symmetry in the trotting horse. Equine Vet J. 2015
33. Parkes RS, Weller R, Groth AM, May S, Pfau T: Evidence of the development of ’domain-restricted’
expertise in the recognition of asymmetric motion characteristics of hindlimb lameness in the horse. Eq.
Vet.J.2009, 41, 112–117.
Head and pelvic movement asymmetries at trot in riding horses in training
PLOS ONE | https://doi.org/10.1371/journal.pone.0176253 April 25, 2017 16 / 16
Available via license: CC BY 4.0
Content may be subject to copyright.
Content uploaded by Thilo Pfau
Author content
All content in this area was uploaded by Thilo Pfau on Jun 28, 2017
Content may be subject to copyright.
