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Article history: Lameness detection can be challenging in dogs, as reflected in the reported low inter-rater agreement
Accepted 8 February 2017 when visually assessing lameness. The aim of this study was to use an inertial sensor-based system to
detect and quantify induced distal and proximal limb disturbances mimicking supporting and swinging
Keywords: limb lameness in dogs trotting on a treadmill by measuring vertical head and pelvic movement sym-
Accelerometer metry. Ten clinically sound dogs were equipped with inertial measurement units that were attached to
Biomechanics
the head, pelvis and right distal forelimb. Vertical head and pelvic movement symmetry were mea-
Canine
sured while dogs trotted on a treadmill, before and after the induction of moderate support or swinging
Inertial motion sensors
Lameness compensatory mechanisms fore- and hindlimb lameness. Four symmetry variables were calculated: the differences in displace-
ment between the two lowest and between the two highest values of the head and pelvis per stride,
respectively. These variables were defined as minimum head difference (HDmin), maximum head dif-
ference (HDmax), minimum pelvic difference (PDmin) and maximum pelvic difference (PDmax). Induction
of supporting forelimb and hindlimb lameness produced significant changes in HDmin and PDmin, re-
spectively. Swinging forelimb and hindlimb lameness produced significant changes in HDmax and PDmax,
respectively. Additional compensatory ipsilateral forelimb and contralateral hindlimb movements were
detected. Based on our findings, inertial sensor-based systems can be used to detect and quantify induced
moderate lameness and differentiate between supporting and swinging limb lameness in dogs trotting
on a treadmill. Further studies are needed to evaluate this method in dogs presented for clinical lame-
ness evaluation and in overground locomotion.
© 2017 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction These results are confirmed by those of another study, where clin-
ically lame dogs were studied after tibial osteotomy repair (Quinn
Lameness evaluation can be challenging in dogs. It aims to iden- et al., 2007). In light of these findings, there is an increased inter-
tify the lame limb(s), by scoring the degree of lameness and localising est in better understanding canine lameness by using more precise
the origin of the pain or discomfort. Lameness can be classified as and objective methods of assessment. Several kinetic and kinemat-
supporting or swinging limb lameness, as defined by Houlton (2006) ic studies have recently been performed in dogs with induced
as ‘reluctance or inability to place full weight on the limb’ and ‘lame- lameness (Waxman et al., 2008; Bockstahler et al., 2009; Katic et al.,
ness seen when the affected limb is in flight’, respectively. Waxman 2009; Abdelhadi et al., 2012, 2013; Fischer et al., 2013) and in lame
et al. (2008) measured ground reaction forces in dogs with induced canine patients (Hicks and Millis, 2014). A recent kinematic study
supporting lameness, after visual scoring by three small animal or- in dogs with experimentally induced lameness, performed with a
thopaedic surgeons and three first year veterinary students. The motion capture system, demonstrated that symmetry measure-
agreement between the visual assessment and the force platform ments of vertical head and pelvic movement, which are clinical
data was low (0–39% agreement), depending on the degree of lame- variables commonly used in visual lameness assessment, were
ness. The authors concluded that subjective evaluation of lameness enough to identify the lame limb (Gómez Álvarez et al., 2017). The
varied greatly between observers and that it agreed poorly with ob- study also identified, for the first time in dogs, additional head and
jective measures of limb function, such as ground reaction forces. pelvic compensatory lameness mechanisms (i.e. head motion for
hindlimb lameness and pelvic motion for forelimb lameness). These
compensatory movements may further contribute to the marked
* Corresponding author. variability between clinicians during visual evaluation of canine
E-mail address: marie.rhodin@slu.se (M. Rhodin). lameness (Waxman et al., 2008).
http://dx.doi.org/10.1016/j.tvjl.2017.02.004
1090-0233/© 2017 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/
4.0/).
M. Rhodin et al. / The Veterinary Journal 222 (2017) 54–59 55
Table 1
Descriptive statistics for fore- and hindlimb lameness parameters.
SD, standard deviation; HDmin, minimum head difference; HDmax, maximum head difference; PDmin, minimum pelvic difference; PDmax, maximum pelvic difference.
a
Number of dogs from the total of 10 with either a left (−) or right (+) limb asymmetry for each variable.
b Positive (right) or negative (left) values for sound and after lameness induction.
90 trials, each with four asymmetry values measured, with a mean (HDmax) or hindlimb (PDmax) lameness parameters with the ex-
number of strides of 34 ± 7.3. Small pre-existing asymmetries of dif- pected sign (negative for left and positive for right limb lameness
ferent signs were detected (positive or negative values of the induction), with absolute values significantly greater than before
differences in displacement). These were not clinically observable induction in nine of the 10 dogs (Table 1). There was a significant
(Table 1). increase in amplitude for HDmax (negative in the left, −40 ± 21.1;
positive in the right, 36 ± 15.1) (forelimb lameness; P = 0.002) in dogs
Supporting limb lameness with swinging limb lameness in the forelimbs. The induction of
swinging limb lameness in the hindlimbs significantly increased the
The Lameness Locator successfully identified the induction of sup- amplitude of PDmax (i.e. negative for left, −11 ± 9.3; positive for right,
porting limb lameness for all limbs in all dogs by measuring changes 11 ± 12.2; P = 0.002). Box plots were drawn, where the median, lowest
in the forelimb (HDmin) or the hindlimb (PDmin) lameness pa-
rameters with the expected sign (negative for left and positive for
right limb lameness), with absolute values significantly greater than
before induction (Table 1).
There was a significant change in HDmin (mean ± SD) in dogs
with supporting lameness in the forelimbs when left (−40 ± 25.7)
and right (43 ± 27.0) forelimb lameness was induced (P = 0.002). In-
duction of supporting lameness in the left hindlimb significantly
increased the amplitudes of PDmin (−12 ± 7.9) and PDmax
(−9.1 ± 14.1; P = 0.03) and induction in the right hindlimb also in-
creased the amplitude of PDmin (11 ± 7.6) significantly (P = 0.002).
Box plots were drawn, where the median, lowest and highest
quartiles and minimum and maximum values are presented for each
variable (Figs. 2–5). Table 1 presents descriptive statistics.
Swinging limb lameness Fig. 2. Box plots of minimum head difference (HDmin) values before (sound) and
after supporting limb induced lameness on each limb (left forelimb, LF; right fore-
limb, RF; left hindlimb, LH; right hindlimb, RH). Significant differences compared
The Lameness Locator also successfully identified the induc- to sound measurement are indicated by *P = 0.002 for LF and RF induction and
tion of swinging limb lameness by measuring changes in forelimb P = 0.049 for LH induction.
M. Rhodin et al. / The Veterinary Journal 222 (2017) 54–59 57
Fig. 3. Box plots of maximum head difference (HDmax) before (sound) and after sup- Fig. 7. Box plots of maximum head difference (HDmax) values before (sound) and
porting limb induced lameness on each limb (left forelimb, LF; right forelimb, RF; after swinging limb induced lameness on each limb (left forelimb, LF; right fore-
left hindlimb, LH; right hindlimb, RH). No significant differences compared to sound limb, RF; left hindlimb, LH; right hindlimb, RH). Significant differences compared
measurement were detected. to sound measurement are indicated by *P = 0.002 for LF, RF and RH induction.
and highest quartiles and minimum and maximum values are pre-
sented for each variable (Figs. 6–9).
Fig. 8. Box plots of minimum pelvic difference (PDmin) values before (sound) and
Fig. 5. Box plots of maximum pelvic difference (PDmax) values before (sound) and after swinging limb induced lameness on each limb (left forelimb, LF; right fore-
after supporting limb induced lameness on each limb (left forelimb, LF; right fore- limb, RF; left hindlimb, LH; right hindlimb, RH). No significant differences compared
limb, RF; left hindlimb, LH; right hindlimb, RH). Significant differences compared to sound measurement were detected.
to sound measurement are indicated by *P = 0.03 for LH induction.
Fig. 6. Box plots of minimum head difference (HDmin) values before (sound) and Fig. 9. Box plots of maximum pelvic difference (PDmax) values before (sound) and
after swinging limb induced lameness on each limb (left forelimb, LF; right fore- after swinging limb induced lameness on each limb (left forelimb, LF; right fore-
limb, RF; left hindlimb, LH; right hindlimb, RH). Significant differences compared limb, RF; left hindlimb, LH; right hindlimb, RH). Significant differences compared
to sound measurement are indicated by *P = 0.02 for LH induction. to sound measurement are indicated by *P = 0.002 for LH and RH induction.
58 M. Rhodin et al. / The Veterinary Journal 222 (2017) 54–59
consistent with ipsilateral compensatory forelimb movement some degree of asymmetry is evident even in non-lame dogs
asymmetry. (Budsberg et al., 1993; Besancon et al., 2003; Fanchon and Grandjean,
2007; Colborne, 2008; Oosterlinck et al., 2011). When using the
Discussion motion analysis system in horses, there are established threshold
values for asymmetry, i.e. +/−6 mm for the head movement (HDmin
In the present study, induced lameness was successfully de- or HDmax) and +/−3 mm for the pelvic motion (PDmin or PDmax).
tected from head and pelvic movements using inertial motion Corresponding canine values require further investigation. Whether
sensors. Changes in the symmetry between the lowest head and the asymmetry is caused by pain can only be determined by a thor-
pelvic displacements were good indicators of supporting limb ough clinical examination. Further studies in larger populations of
lameness and changes in the symmetry of the highest head and sound and lame dogs are needed to investigate the biological vari-
pelvic displacement indicated swinging limb lameness. Bell et al. ation of motion asymmetries in dogs.
(2016) reported in a study of hindlimb lame horses that the The lameness score of 2 used in the dogs we studied was chosen
difference between the lowest pelvic positions indicated a support- based on the inter-observer variability that exists in dogs during
ing limb lameness, with decreases in loading during the first half the clinical assessment of mild to moderate lameness. Moreover,
of the stance phase, and differences between the maximum pelvic this IMU system uses all the strides recorded and averages them
positions indicated a push off-type lameness, with decreased to produce the results, in contrast with visual lameness scoring in
transfer of vertical force to horizontal force in the second half of dogs, which by definition does not necessarily include all strides
the stance phase. We do not know how our swinging limb (i.e. dogs might not be lame in all strides). In a kinematic study per-
lameness corresponded to specific clinical diagnoses, but we can formed in dogs with subtle clinical lameness by Hicks and Millis
speculate that, as in horses, changes in the symmetry of the (2014), only the pelvis showed significant vertical displacement, not
highest positions of head and pelvis could indicate a push off-type the head. An IMU system should be able to detect more subtle lame-
lameness. The system used was also able to detect compensatory ness than the moderate lameness induced in our study, as it detected
lameness mechanisms other than those expected for the lame small asymmetries in sound limbs; however, further studies on subtle
limb (i.e. head asymmetry for forelimb lameness and pelvic motion lameness are needed to fully explore this.
asymmetry for hindlimb lameness). Therefore, asymmetrical move- In the present study, all dogs were measured during steady state
ment of the head can be considered an indicator of both hindlimb locomotion with very regular motion on a treadmill at a constant
and forelimb lameness. This may contribute to the low inter- speed that yielded measurements with low variability of the head
observer agreement for lameness assessment, and potentially to and pelvic vertical displacement. Sensors can also be used for
misdiagnosis of the correct limb, at least with inexperienced overground measurements, however, it is possible that the regu-
observers. larity of speed and motion will be more difficult to achieve in dogs
Our results agree with our parallel kinematic study, where the during overground measurements compared to horses, but this is
symmetry of vertical head and pelvic motion was described through yet to be established. The dogs used in the study were all medium
optical-based 3D kinematic analysis that was performed simulta- to large size and there were no indications of that gait affected by
neously in these dogs (Gómez Álvarez et al., 2017). Differences in the additional weight of each sensor (30 g). However, this might not
the lowest and highest head and pelvic displacements obtained with be the case in small dog breeds.
both sensors and optical-based kinematic analysis agreed with the Our findings with induced lameness in dogs suggest that similar
lameness induced, confirming that head and pelvic displacements motion patterns might occur in clinical cases, both for supporting
are important symmetry variables for objective lameness evalua- and swinging limb lameness. Further studies are needed to inves-
tions in dogs. The same variables are often used in inertial sensor- tigate whether using IMUs during overground locomotion in clinical
based lameness evaluations in horses (Keegan et al., 2011; Starke settings with lame canine patients will yield the same results.
et al., 2013; Pfau et al., 2015).
Kinetic compensatory lameness mechanisms have been de-
scribed in dogs (Waxman et al., 2008; Bockstahler et al., 2009; Katic Conclusions
et al., 2009; Abdelhadi et al., 2012, 2013; Fischer et al., 2013), dem-
onstrating that compensation occurs by changing the ground reaction Inertial sensor-based systems can successfully be used to detect
forces of the ipsilateral and contralateral limbs, specifically braking, and quantify moderate induced lameness and differentiate between
propulsion, peak vertical force and vertical impulse during fore- and supporting and swinging limb lameness in dogs trotting on a tread-
hindlimb lameness. These changes unload the painful limb, and they mill. If concurrent ipsilateral fore- and hindlimb lameness is
can only be achieved by dynamic postural adaptations of the head, observed, it is possible that the forelimb lameness is a compensa-
trunk and limbs, with subsequent changes in their motion pat- tory lameness rather than a primary lameness. Therefore, the use
terns. This was shown in experimentally induced lameness by Gómez of IMUs might help improve the diagnosis of lameness in dogs and
Álvarez et al. (2017), where an ipsilateral compensatory forelimb also provide a wireless and portable device for the objective quan-
asymmetry was observed during supporting hindlimb lameness in- tification of lameness.
duction. If the same mechanisms exist in clinical cases, there could
be a risk of the clinician targeting the evaluation towards a ‘false’
forelimb lameness. Therefore, when an ipsilateral forelimb and Conflict of interest statement
hindlimb lameness is seen concurrently, with no obvious clinical
findings to explain a true forelimb lameness, the forelimb lame- None of the authors of this paper has financial or personal re-
ness signs might be merely compensatory. However, subtle lationship with other people or organisations that could
contralateral hindlimb asymmetry, observed during forelimb sup- inappropriately influence or bias the content of the paper.
porting lameness, would not lead to confusion or misdiagnosis,
because of the large differences in the magnitudes of the asymme-
tries of the head and pelvis. Acknowledgements
Small pre-existing asymmetries were observed in the dogs before
any lameness had been induced, similar to previous findings in sound We wish to thank Agria Sweden research fund for funding this
dogs evaluated with a diverse array of methods, confirming that study (N2014-0022).
M. Rhodin et al. / The Veterinary Journal 222 (2017) 54–59 59
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