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Naturally-occurring forelimb lameness in the horse results in significant compensatory load redistribution during trotting
The Veterinary Journal 204 (2015) 208–213
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The Veterinary Journal j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / t v j l
Naturally-occurring forelimb lameness in the horse results in significant compensatory load redistribution during trotting Sylvia Maliye, Lance C. Voute, John F. Marshall * Weipers Centre Equine Hospital, School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK
A R T I C L E
I N F O
Article history: Accepted 2 March 2015 Keywords: Diagnostic anaesthesia Horse Kinematics Lameness Orthopaedics
A B S T R A C T
This study aimed to quantify the compensatory response to naturally-occurring forelimb lameness on load redistribution. Data from lameness investigations using an inertial sensor based system to monitor the response to forelimb diagnostic anaesthesia were reviewed. Horses with primary forelimb lameness were grouped for analysis as (1) all horses combined (n = 28), (2) forelimb-only lameness (n = 8/28), (3) forelimb–contralateral hindlimb lameness (n = 14/28), (4) forelimb–ipsilateral hindlimb lameness (n = 6/28). The effect of diagnostic anaesthesia on measures of head and pelvic movement asymmetry was determined using the Wilcoxon signed rank test. Spearman’s correlation analysis was performed between forelimb and hindlimb variables. Statistical significance was set at P < 0.05. Forelimb diagnostic anaesthesia resulted in a decrease in pelvic movement asymmetry among all horses and the forelimb-only and forelimb–contralateral hindlimb lameness groups. Pelvic movement asymmetry associated with the contralateral hindlimb decreased by a median of 38% (interquartile range [IQR] 10–65%), 43% (IQR 28–60%) and 28% (IQR 12–67%) in all horses, forelimb-only and forelimb–contralateral hindlimb groups respectively (P < 0.05). Maximum pelvic height difference (PDMax) significantly decreased in all horses combined and the forelimb–contralateral hindlimb lameness group by a median of 66% (IQR 24–100%) and 78% (IQR 27–100%, P < 0.01), respectively. Change in head movement asymmetry and vector sum was significantly positively correlated with PDMax in all horses combined and the forelimb–contralateral hindlimb group (P < 0.05). Forelimb lameness had a significant effect on hindlimb and pelvic movement in horses with clinical lameness resulting in compensatory load redistribution and decreased push-off from the contralateral hindlimb. © 2015 Elsevier Ltd. All rights reserved.
Introduction Compensatory load redistribution as a result of primary forelimb or hindlimb lameness is a well-recognised phenomenon that can result in a clinical observation of ‘false’ or compensatory lameness and potentially lead to misdiagnosis. Variable patterns of compensatory load redistribution have been identified in small numbers of horses with forelimb lameness during treadmill examination (Buchner et al., 1996a; Uhlir et al., 1997; Vorstenbosch et al., 1997; Weishaupt et al., 2004, 2006; Kelmer et al., 2005); both weightbearing ipsilateral hindlimb lameness (Weishaupt et al., 2006) and contralateral hindlimb lameness (Uhlir et al., 1997) have been reported. The current study aimed to extend these observations to horses with naturally-occurring forelimb lameness during routine clinical examination. Inertial sensor-based systems are sensitive, repeatable and accurate, allowing quantitative gait analysis to be performed during
* Corresponding author: Tel.: +44 141 330 5999. E-mail address: [email protected] (J.F. Marshall). http://dx.doi.org/10.1016/j.tvjl.2015.03.005 1090-0233/© 2015 Elsevier Ltd. All rights reserved.
clinical lameness examinations including diagnostic anaesthesia (Marshall et al., 2012; Maliye et al., 2013). By examining the effect of alleviating forelimb lameness on ipsilateral and contralateral hindlimb movement during weight bearing and push-off, we aimed to further characterise the relationship between forelimb lameness and compensatory load redistribution. We hypothesised that naturally-occurring forelimb lameness would result in contralateral hindlimb asymmetry that could be interpreted as lameness. Furthermore, we hypothesised that alleviating clinical lameness through diagnostic anaesthesia would result in improvement to contralateral hindlimb asymmetry, but not ipsilateral hindlimb asymmetry. Materials and methods Medical record review Medical records of horses that underwent lameness investigation between September 2011 and October 2013 that included the use of an inertial sensor-based system (Lameness Locator, Equinosis LLC) were reviewed retrospectively. Horses that underwent diagnostic anaesthesia that resulted in a significant improvement in forelimb lameness were included for further analysis.
S. Maliye et al./The Veterinary Journal 204 (2015) 208–213
Kinematic lameness analysis A commercially available inertial sensor system (Lameness Locator, Equinosis LLC) objectively evaluated lameness by measuring eight parameters, as previously described (Keegan et al., 2011; Marshall et al., 2012; Maliye et al., 2013). Kinematic data were collected at the trot only and a minimum of 30 strides were required for the data to be accepted for the study. The mean difference (mm) in maximum head height after the stance phases of the right and left forelimbs and, similarly, the minimum head height representing the difference (mm) in minimum head height during the stance phases of the right and left forelimbs were recorded. Similarly, the mean difference (mm) in maximum pelvic height after the stance phases of the right and left hindlimbs and the minimum pelvic height representing the difference (mm) in minimum pelvic height during the stance phases of the right and left hindlimbs were recorded. Additionally, general measures of vertical head movement asymmetry and pelvic movement asymmetry were calculated and assigned to either right or left forelimbs and hindlimbs, respectively. Negative values were assigned to the left and positive values to the right limb. These measures of head and pelvic movement asymmetry are expressed as a ratio without units, as previously described (Keegan et al., 2001).
Lameness examinations and diagnostic anaesthesia All horses included in the study underwent a complete examination by a veterinarian specialising in equine lameness (JFM or LCV), including a minimum of walk and trot in a straight line and lunging in a circle in both directions on hard and soft surfaces. The primary lame limb was subjectively identified and the severity of lameness graded according to the American Association of Equine Practitioners (AAEP) scale (0–5).1 Because examination of lameness during trotting was an inclusion criterion, only horses with a forelimb lameness of grade 3 or less on the AAEP scale were included in the study. Horses were included in further analysis only if the following objective conditions for confirmation of forelimb lameness were met: (1) head movement asymmetry of greater than 0.5, and (2) maximum and/or minimum head height of >±6 mm. For all horses, the presence or absence of lameness was determined subjectively and objectively for all limbs. Hindlimb lameness was defined as a subjective AAEP lameness score of between 1 and 3 and the following objective conditions: (1) pelvic movement asymmetry of >0.17 and (2) maximum or minimum pelvic height of >±3 mm. Immediately prior to diagnostic anaesthesia each horse was trotted in a straight line on a level concrete surface with a loose lead rope to collect baseline kinematic data. Skin sensation on the distal limb was tested as part of the physical examination using a blunt probe prior to performing regional anaesthesia. Thereafter, the diagnostic anaesthesia procedure was performed as determined by the clinician (JFM or LCV). Following confirmation of desensitised by application of blunt pressure distal to the site of diagnostic anaesthesia, the horse was again trotted in a straight line (anaesthesia examination) in a similar manner to the control (baseline) examination. In cases where an intra-articular local anaesthesia block was performed the horse was trotted 10 min following the procedure. The response to the diagnostic anaesthesia was categorised by both subjective observation of improvement in gait by the clinician and also a change in objective kinematic data as previously described (Maliye et al., 2013). Briefly, a positive response was defined as: (1) a decrease in head movement asymmetry of the blocked limb to below 0.5; (2) a decrease in mean difference in maximum and/or minimum head height of >50%. Only those horses for which a positive response was confirmed both subjectively and objectively were included in the study.
Classification of lameness The primary lame limb was determined by the clinician performing the examination and horses were subsequently classified according to lameness detected in other limbs. This classification was based on the clinical scenarios of forelimb lameness only, concurrent forelimb and contralateral hindlimb lameness, and concurrent forelimb and ipsilateral hindlimb lameness. Therefore, data analysis was performed for all horses combined prior to analysis of groups consisting of (1) primary forelimb lameness only; (2) primary forelimb–contralateral hindlimb lameness, or (3) primary forelimb–ipsilateral hindlimb lameness.
Data analysis For all examinations, the vector sum of maximum and minimum head height was calculated as √([ maximum head height]2 + [ minimum head height]2) and assigned to the left or right side depending on whether minimum head height was positive or negative (Keegan et al., 2012). A Shapiro–Wilk normality test was
1 See: http://www.aaep.org/info/horse-health?publication=836 (accessed 25 February 2015).
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performed prior to data analysis. All parameters were described as median and interquartile range (IQR). The median and interquartile range of the percentage change in each parameter following diagnostic anaesthesia were calculated. Baseline measures of head and pelvic movement asymmetry were compared between groups using an ANOVA on ranks with Dunn’s post hoc test. The effect of diagnostic anaesthesia on all horses combined and within each group (forelimb-only, forelimb–contralateral hindlimb, forelimb–ipsilateral hindlimb) on all kinematic parameters was determined by Wilcoxon signed rank test. All statistical analyses were performed using commercially available software (SigmaPlot 11.2, Systat Software LLC). The correlation between the changes in measures of forelimb and hindlimb asymmetry following forelimb diagnostic anaesthesia was determined by performing Spearman’s rank correlation analysis. Correlation analysis was performed for each group (all horses, forelimb-only, forelimb–contralateral hindlimb, forelimb–ipsilateral hindlimb). Statistical significance was set at P < 0.05.
Results Medical record review A total of 28 horses with primary forelimb lameness met the inclusion criteria for this study and were grouped as follows: forelimbonly (n = 8), forelimb–contralateral hindlimb (n = 14), and forelimb– ipsilateral hindlimb (n = 6) (Table 1). Comparison of forelimb lameness between groups There was no significant difference in baseline measures of forelimb movement asymmetry between any of the groups (Table 2).
Table 1 Table describing the affected forelimb, diagnostic anaesthesia technique, and diagnosis of horses included in the study. Horse
Group
Forelimb
Diagnostic anaesthesia
Diagnosis
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
FO FO FO FO FO FO FO FO FC FC FC FC FC FC FC FC FC FC
RF RF RF LF LF LF LF RF LF LF LF RF LF RF LF LF LF RF
Palmar heel pain Pedal bone fracture Navicular disease Navicular disease DIPJ OA DDFT tear DIPJ OA DFTS synovitis Navicular disease DDFT tendonitis DDFT tendonitis DIPJ OA Unilateral laminitis Navicular disease SSL desmitis MCPJ OA DDFT tear SDFT tendonitis
19
FC
LF
20 21 22 23 24 25 26
FC FC FC FI FI FI FI
RF LF LF LF RF LF RF
27 28
FI FI
LF LF
PD PD AS AS AS AS DIPJ DFTS PD PD PD PD AS AS AS Low 4 point Low 4 point Median and ulnar nerves Median and ulnar nerves DFTS Radiocarpal joint Intercarpal joint PD PD AS Lateral palmar nerve DIPJ MCPJ
MCII osteopathy DDFT tendonitis Radiocarpal joint OA Intercarpal joint OA Navicular disease Navicular disease PIPJ OA SL desmitis DIPJ OA MCPJ OA
FO, forelimb-only lameness; FC, forelimb–contralateral hindlimb lameness; FI, forelimb–ipsilateral hindlimb lameness; LF, left forelimb; RF, right forelimb; PD, palmar digital; AS, abaxial sesamoid; DIPJ, distal interphalangeal joint; PIPJ, proximal interphalangeal joint; SDFT, superficial digital flexor tendon; DDFT, deep digital flexor tendon DDFT; DFTS, digital flexor tendon sheath; SL, suspensory ligament; SSL, straight sesamoidean ligament; MCPJ, metacarpophalangeal joint; OA, osteoarthritis.
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Table 2 The effect of diagnostic anaesthesia (blocking) of a forelimb on measures of forelimb asymmetry. Data are presented as the median and interquartile range. Group Parameter
Forelimb
Examination
All
FO
FC
FI
HMA
Blocked
Baseline Anaesthesia Baseline Anaesthesia Baseline Anaesthesia
0.84 (0.68–1.26) 0.43b (0.26–0.62) 0.02 (0.00–0.07) 0.13b (0.07–0.39) 18.25 (12.17–31.99) 5.22b (−5.36–12.15)
0.70 (0.61–1.09) 0.32a (0.01–0.583) 0.03 (0.00–0.06) 0.16a (0.11–0.67) 15.28 (12.17–27.10) −3.03a (−12.30–6.77)
1.14 (0.72–1.57) 0.54a (0.31–0.85) 0.017 (0.00–0.39) 0.11a (0.05–0.22) 30.25 (13.74–38.86) 11.61a (6.06–15.05)
0.70 (0.68–0.81) 0.33a (0.21–0.443) 0.07 (0.04–0.132) 0.39a (0.12–0.65) 14.19 (9.84–15.75) 6.78b (−13.29–4.39)
Contralateral VS (mm)
HMA, head movement asymmetry; VS, vector sum; All, all horses combined; FO, forelimb-only lameness; FC, forelimb–contralateral hindlimb lameness; FI, forelimb– ipsilateral hindlimb lameness. a Significant difference (P < 0.05) compared with baseline examination. b Significant difference (P < 0.01) compared with baseline examination.
Effect of diagnostic anaesthesia on forelimb kinematic parameters in horses with primary forelimb lameness There was a significant decrease in both the head movement asymmetry assigned to the blocked forelimb and vector sum in all of the four groups following diagnostic anaesthesia (Table 2). There was a significant increase in head movement asymmetry assigned to the contralateral forelimb in all of the four groups (Table 2). Effect of diagnostic anaesthesia on hindlimb kinematic parameters in horses with primary forelimb lameness In all horses combined and within the forelimb-only and forelimb–contralateral hindlimb groups, there was a significant decrease in the pelvic movement asymmetry assigned to the contralateral hindlimb, and a significant increase in the pelvic movement asymmetry assigned to the ipsilateral hindlimb following diagnostic anaesthesia (P < 0.05, Table 3). The contralateral hindlimb pelvic movement asymmetry decreased by a median of 38% (IQR 10–65%), 43% (IQR 28–60%) and 28% (IQR 12–67%) in all horses combined, forelimb-only and forelimb–contralateral hindlimb groups respectively. There was no significant effect of diagnostic anaesthesia on pelvic movement asymmetry of the contralateral or ipsilateral hindlimb in the forelimb–ipsilateral hindlimb group. Maximum pelvic height significantly decreased in all horses combined and within the forelimb–contralateral hindlimb group by a median of 66% (IQR 24–100%) and 78% (IQR 27–100%) respectively (P < 0.01). There was no significant effect of diagnostic anaesthesia on minimum pelvic height in any group (Table 3). Correlation analysis revealed significant positive correlations between the change in head movement asymmetry of the blocked limb and the contralateral hindlimb pelvic movement asymmetry (Figs. 1A, B) and between the change in vector sum and
the contralateral hindlimb pelvic movement asymmetry in all horses combined and within the forelimb-only and forelimb–contralateral hindlimb groups. In all horses combined and within the forelimbonly group a significant negative correlation was identified between the change in head movement asymmetry of the blocked forelimb and the pelvic movement asymmetry of the ipsilateral hindlimb and between the vector sum and the pelvic movement asymmetry of the ipsilateral hindlimb. There were significant positive correlations between the change in the head movement asymmetry of the blocked limb and the change in maximum pelvic height and the change in vector sum and the change in maximum pelvic height in all horses combined and within the forelimb-only group (Figs. 1B, C). Significant results of the correlation analysis are summarised in Table 4. Discussion The purpose of this study was to investigate compensatory load redistribution in clinical equine lameness by objectively examining the effect of reducing lameness through diagnostic anaesthesia. By measuring kinematic parameters prior to and following diagnostic anaesthesia, we have demonstrated the effect of lameness on the other limbs in horses with naturally occurring lameness under clinical examination conditions. This is in contrast to earlier studies that used experimentally-induced lameness and/or treadmill examination as a model of load re-distribution (Buchner et al., 1996a, 1996b; Uhlir et al., 1997; Kelmer et al., 2005; Weishaupt et al., 2006; Orito et al., 2007). We have demonstrated that a significant proportion of forelimb lameness cases have a concurrent compensatory lameness that is improved by diagnostic anaesthesia of the primary lame limb. Of the 28 horses included in our study, a total of 14/28 (50%) had subjective and objective evidence of forelimb and contralateral hindlimb
Table 3 The effect of diagnostic anaesthesia (blocking) of a forelimb on measures of hindlimb asymmetry. Data are presented as the median and interquartile range. Group Parameter
Hindlimb
Examination
All
FO
FC
FI
PMA
Ipsilateral
Baseline Anaesthesia Baseline Anaesthesia Baseline Anaesthesia Baseline Anaesthesia
0.06 (0.02–0.15) 0.14a (0.05–0.23) 0.18 (0.10–0.28) 0.08a (0.05–0.21) 3.62 (1.88–7.18) 1.34b (−0.63–3.65) 1.84 (0.76–5.51) 1.54 (−0.40–5.76)
0.07 (0.05–0.11) 0.15a (0.13–0.16) 0.14 (0.10–0.16) 0.07a (0.05–0.11) 1.79 (0.68–2.9) 1.34 (−1.26–2.22) 1.04 (0.67–1.48) 0.10 (−1.62–0.95)
0.02 (0.00–0.03) 0.05a (0.01–0.13) 0.28 (0.22–0.36) 0.21a (0.07–0.27) 7.18 (4.76–10.45) 1.63a (−0.23–5.22) 2.32 (0.77–5.05) 1.82 (−0.47–6.08)
0.23 (0.19–0.25) 0.26 (0.23–0.34) 0.07 (0.04–0.08) 0.02 (0.00–0.08) 2.46 (1.13–3.69) 1.03 (−5.09–2.79) 6.00 (4.26–6.56) 6.30 (3.77–7.39)
Contralateral PDMax (mm) PDMin (mm)
All, all groups combined; FO, forelimb-only lameness; FC, forelimb–contralateral hindlimb lameness; FI, forelimb–ipsilateral hindlimb lameness; PMA, pelvic movement asymmetry; PDMax, mean difference in millimetres in maximum pelvic height after the stance phases of the right and left hindlimbs; PDMin, mean difference in millimetres in minimum pelvic height during the stance phases of the right and left hindlimbs. a Significant difference (P < 0.05) compared with baseline examination. b Significant difference (P < 0.01) compared with baseline examination.
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Fig. 1. Scatter plots of the results of Spearman’s rank correlation analysis. There was a significant correlation between HMA associated with the blocked limb and PMA associated with the contralateral hindlimb in those horses with forelimb lameness only group (A, r = 0.95, P < 0.01) and horses with forelimb–contralateral hindlimb lameness (B, r = 0.68, P < 0.01). There was a significant correlation between vector sum and PDMax in all horses combined (C, r = 0.54, P < 0.01) and horses with forelimb– contralateral hindlimb lameness (D, r = 0.80, P < 0.01). HMA, measure of vertical head movement asymmetry assigned to either the right or left forelimb depending on the sign (±) of HDMin with negative values assigned to the left and positive values to the right limb. HDMax, mean difference in millimetres in maximum head height after the stance phases of the right and left forelimbs. HDMin, mean difference in millimetres in minimum head height during the stance phases of the right and left forelimb. VS, measure of head movement asymmetry, defined as √(HDMax)2 + (HDMin)2. PMA, measure of vertical head movement asymmetry assigned to either the right or left hindlimb depending on the sign (±) of PDMin with negative values assigned to the left and positive values to the right limb. PDMax, mean difference in millimetres in maximum pelvic height after the stance phases of the right and left hindlimbs. PDMin, mean difference in millimetres in minimum pelvic height during the stance phases of the right and left hindlimbs.
lameness. A total of 6/28 (21%) of horses had evidence of forelimb and ipsilateral hindlimb lameness. While the high proportion of multi-limb lameness cases reported may reflect the caseload of our referral hospital, it does illustrate the importance of identifying the primary lame limb prior to commencing lameness investigation with diagnostic anaesthesia. Similar to a previous study (Maliye et al., 2013), we found a significant effect of diagnostic anaesthesia on kinematic parameters of movement asymmetry following diagnostic anaesthesia of the lame forelimb. While the previous study was limited to horses with forelimb lameness only, our findings demonstrate the objective detection of a positive response to diagnostic anaesthesia in horses under investigation for multi-limb lameness. Moreover, we have demonstrated the objective assessment of perineural diagnostic anaesthesia proximal to the foot and intra-synovial anaesthesia. There was a significant alteration in pelvic movement asymmetry associated with both hindlimbs in all horses and both the
forelimb-only and forelimb–contralateral hindlimb lameness groups following diagnostic anaesthesia. Specifically, the pelvic movement asymmetry assigned to the contralateral hindlimb decreased while pelvic movement asymmetry assigned to the ipsilateral hindlimb increased. Furthermore, there was a significant correlation between the improvement in head movement asymmetry and improvement in pelvic movement asymmetry following diagnostic anaesthesia. A correlation between induced change in head movement and pelvic movement has been previously reported (Kelmer et al., 2005). Interestingly, the strength of the correlations was much greater in the current clinical study despite the standardised methods of the previous experimental treadmill experiment (Kelmer et al., 2005). Improvement in contralateral limb asymmetry was previously reported following diagnostic anaesthesia of forelimb lameness localised to the foot (Maliye et al., 2013). However, that study did not investigate further the reasons for this improved contralateral hindlimb asymmetry.
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Table 4 Spearman’s rank correlation analysis of the change in parameters of forelimb and hindlimb asymmetry following diagnostic anaesthesia. Spearman’s rank correlation coefficient, r, and the corresponding P values are provided for statistically significant correlations only. Group All All All All All All FO FO FO FO FC FC FC FC FI
Comparison
r value
P value
HMA (blocked limb) vs. PMA (contralateral hindlimb) HMA (blocked limb) vs. PMA (ipsilateral hindlimb) HMA (blocked limb) vs. PDMax VS vs. PMA (contralateral hindlimb) VS vs. PMA (ipsilateral hindlimb) VS vs. PDMax HMA (blocked limb) vs. PMA (contralateral hindlimb) HMA (blocked limb) vs. PMA (ipsilateral hindlimb) VS vs. PMA (contralateral hindlimb) VS vs. PMA (ipsilateral hindlimb) HMA (blocked limb) vs. PMA (contralateral hindlimb) HMA (blocked limb) vs. PDMax VS vs. PMA (contralateral hindlimb) VS vs. PDMax VS vs. PMA (contralateral hindlimb)
0.68 −0.53 0.60 0.55 −0.39 0.54 0.95 −0.86 0.71 −0.83 0.68 0.74 0.71 0.80 0.94
<0.01 <0.01 <0.01 <0.01 <0.05 <0.01 <0.01 <0.01 <0.05 <0.01 <0.01 <0.01 <0.05 <0.01 <0.05
All, all horses combined; FO, forelimb-only lameness; FC, forelimb–contralateral hindlimb lameness; FI, forelimb–ipsilateral hindlimb lameness; HMA, head movement asymmetry; VS, vector sum; PMA, pelvic movement asymmetry; PDMax, mean difference in millimetres in maximum pelvic height after the stance phases of the right and left hindlimbs; PDMin, mean difference in millimetres in minimum pelvic height during the stance phases of the right and left hindlimbs.
Our study demonstrated that in clinical cases of forelimb lameness there was a significant decrease in the difference in maximum pelvic height after the stance phase of the left and right hindlimbs associated with a positive response to diagnostic anaesthesia. Furthermore, in all horses with forelimb lameness and among those with concurrent contralateral hindlimb lameness there was a significant correlation between the change in measures of forelimb asymmetry and the difference in maximum pelvic height after the stance phase of the left and right hindlimbs i.e. push-off. This implies that compensatory lameness or load re-distribution in these groups is associated with the push-off component of the stride rather than impact and loading. Specifically, forelimb lameness resulted in a decrease in push-off from the contralateral hindlimb that was improved by diagnostic anaesthesia. Previous experimental studies have demonstrated a shift in loading from the lame forelimb to the diagonal hindlimb (Vorstenbosch et al., 1997; Weishaupt et al., 2006). In the present study, diagnostic anaesthesia resulted in a significant increase in loading of the forelimb (decreased vector sum) that was significantly correlated with an increase in push-off (decreased difference in maximum pelvic height after stance phase of hindlimbs) from the contralateral hindlimb. Therefore, the reduction in hindlimb push-off associated with forelimb lameness is most likely a reflection of increased loading of the hindlimb. Previous studies have disagreed about whether forelimb lameness results in a compensatory weight-bearing ipsilateral hindlimb lameness (Weishaupt et al., 2006), or a contralateral hindlimb lameness (Uhlir et al., 1997) using ground-reaction force measurement and kinematics, respectively. There was no significant change in the difference in minimum pelvic height during stance phase between the left and right hindlimbs following diagnostic anaesthesia, nor a correlation between minimum pelvic height and either of the measures of forelimb asymmetry in any group. In addition, pelvic movement asymmetry associated with the ipsilateral hindlimb was actually observed to increase significantly following diagnostic anaesthesia in all groups except those horses with forelimb lameness and ipsilateral hindlimb lameness. We were therefore unable to identify evidence of compensatory ipsilateral weight-bearing lameness in this population of horses. The current study of naturally occurring lameness during a clinical examination suggests that a reduction in push-off from the contralateral hindlimb in cases of forelimb
lameness can result in perceived false or compensatory contralateral hindlimb lameness. In the current study, the purpose of analysing the horses as subgroups was to investigate the specific clinical scenarios encountered during lameness investigation. Although there was a significant effect of diagnostic anaesthesia on the forelimb lameness, there was no significant change in any of the measured hindlimb kinematic parameters in the group of horses with concurrent ipsilateral hindlimb lameness. These findings, in combination with the lack of improvement in ipsilateral lameness when all horses were analysed, suggest that the lameness in the ipsilateral hindlimb of these horses was a ‘true’ lameness and not the result of compensatory load distribution. However, this difference may also reflect the differences in experimental methods including the use of inertial sensors rather than a camera based kinematic system, data analysis and horse populations between previous studies and our study. In the current study, the concurrent ipsilateral hindlimb lameness group was the smallest with six horses. This will have reduced the statistical power of the analysis to identify a significant difference in hindlimb parameters. Therefore, a further analysis of a larger group of horses is warranted. The low number of horses reflects the clinical nature of the population as the clinicians involved in this study generally performed diagnostic anaesthesia in the hindlimb of horses with ipsilateral forelimb and hindlimb lameness. Overall, the analysis of forelimb diagnostic anaesthesia provides significant clinical evidence that forelimb lameness results in significant compensatory load distribution that is manifest as contralateral hindlimb lameness. Furthermore, while a previous study found evidence of compensatory contralateral limb lameness in horses with severe forelimb lameness (Uhlir et al., 1997), we have demonstrated detectable and significant load redistribution in horses with mild or moderate forelimb lameness and both with and without observed hindlimb lameness. Conclusions Our study has expanded upon previously assumed knowledge by characterising the compensatory hindlimb lameness associated with primary forelimb lameness. By objectively examining this population of horses with clinical lameness we have provided strong evidence objectively supporting part of the ‘law of sides’. When assessing the lame horse it is important to eliminate hindlimb lameness as a possible cause of forelimb lameness and vice versa prior to performing further diagnostic techniques. In addition, when assessing the response to diagnostic anaesthesia in horses with forelimb and hindlimb lameness it is useful to define the effect on both the hind and forelimb movements. Conflict of interest statement None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper. Acknowledgements We wish to thank everyone who was involved with helping during lameness examinations undertaken at the Weipers Centre, University of Glasgow. References Buchner, H.H., Savelberg, H.H., Schamhardt, H.C., Barneveld, A., 1996a. Head and trunk movement adaptations in horses with experimentally induced fore- or hindlimb lameness. Equine Veterinary Journal 28, 71–76.
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The Veterinary Journal j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / t v j l
Naturally-occurring forelimb lameness in the horse results in significant compensatory load redistribution during trotting Sylvia Maliye, Lance C. Voute, John F. Marshall * Weipers Centre Equine Hospital, School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK
A R T I C L E
I N F O
Article history: Accepted 2 March 2015 Keywords: Diagnostic anaesthesia Horse Kinematics Lameness Orthopaedics
A B S T R A C T
This study aimed to quantify the compensatory response to naturally-occurring forelimb lameness on load redistribution. Data from lameness investigations using an inertial sensor based system to monitor the response to forelimb diagnostic anaesthesia were reviewed. Horses with primary forelimb lameness were grouped for analysis as (1) all horses combined (n = 28), (2) forelimb-only lameness (n = 8/28), (3) forelimb–contralateral hindlimb lameness (n = 14/28), (4) forelimb–ipsilateral hindlimb lameness (n = 6/28). The effect of diagnostic anaesthesia on measures of head and pelvic movement asymmetry was determined using the Wilcoxon signed rank test. Spearman’s correlation analysis was performed between forelimb and hindlimb variables. Statistical significance was set at P < 0.05. Forelimb diagnostic anaesthesia resulted in a decrease in pelvic movement asymmetry among all horses and the forelimb-only and forelimb–contralateral hindlimb lameness groups. Pelvic movement asymmetry associated with the contralateral hindlimb decreased by a median of 38% (interquartile range [IQR] 10–65%), 43% (IQR 28–60%) and 28% (IQR 12–67%) in all horses, forelimb-only and forelimb–contralateral hindlimb groups respectively (P < 0.05). Maximum pelvic height difference (PDMax) significantly decreased in all horses combined and the forelimb–contralateral hindlimb lameness group by a median of 66% (IQR 24–100%) and 78% (IQR 27–100%, P < 0.01), respectively. Change in head movement asymmetry and vector sum was significantly positively correlated with PDMax in all horses combined and the forelimb–contralateral hindlimb group (P < 0.05). Forelimb lameness had a significant effect on hindlimb and pelvic movement in horses with clinical lameness resulting in compensatory load redistribution and decreased push-off from the contralateral hindlimb. © 2015 Elsevier Ltd. All rights reserved.
Introduction Compensatory load redistribution as a result of primary forelimb or hindlimb lameness is a well-recognised phenomenon that can result in a clinical observation of ‘false’ or compensatory lameness and potentially lead to misdiagnosis. Variable patterns of compensatory load redistribution have been identified in small numbers of horses with forelimb lameness during treadmill examination (Buchner et al., 1996a; Uhlir et al., 1997; Vorstenbosch et al., 1997; Weishaupt et al., 2004, 2006; Kelmer et al., 2005); both weightbearing ipsilateral hindlimb lameness (Weishaupt et al., 2006) and contralateral hindlimb lameness (Uhlir et al., 1997) have been reported. The current study aimed to extend these observations to horses with naturally-occurring forelimb lameness during routine clinical examination. Inertial sensor-based systems are sensitive, repeatable and accurate, allowing quantitative gait analysis to be performed during
* Corresponding author: Tel.: +44 141 330 5999. E-mail address: [email protected] (J.F. Marshall). http://dx.doi.org/10.1016/j.tvjl.2015.03.005 1090-0233/© 2015 Elsevier Ltd. All rights reserved.
clinical lameness examinations including diagnostic anaesthesia (Marshall et al., 2012; Maliye et al., 2013). By examining the effect of alleviating forelimb lameness on ipsilateral and contralateral hindlimb movement during weight bearing and push-off, we aimed to further characterise the relationship between forelimb lameness and compensatory load redistribution. We hypothesised that naturally-occurring forelimb lameness would result in contralateral hindlimb asymmetry that could be interpreted as lameness. Furthermore, we hypothesised that alleviating clinical lameness through diagnostic anaesthesia would result in improvement to contralateral hindlimb asymmetry, but not ipsilateral hindlimb asymmetry. Materials and methods Medical record review Medical records of horses that underwent lameness investigation between September 2011 and October 2013 that included the use of an inertial sensor-based system (Lameness Locator, Equinosis LLC) were reviewed retrospectively. Horses that underwent diagnostic anaesthesia that resulted in a significant improvement in forelimb lameness were included for further analysis.
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Kinematic lameness analysis A commercially available inertial sensor system (Lameness Locator, Equinosis LLC) objectively evaluated lameness by measuring eight parameters, as previously described (Keegan et al., 2011; Marshall et al., 2012; Maliye et al., 2013). Kinematic data were collected at the trot only and a minimum of 30 strides were required for the data to be accepted for the study. The mean difference (mm) in maximum head height after the stance phases of the right and left forelimbs and, similarly, the minimum head height representing the difference (mm) in minimum head height during the stance phases of the right and left forelimbs were recorded. Similarly, the mean difference (mm) in maximum pelvic height after the stance phases of the right and left hindlimbs and the minimum pelvic height representing the difference (mm) in minimum pelvic height during the stance phases of the right and left hindlimbs were recorded. Additionally, general measures of vertical head movement asymmetry and pelvic movement asymmetry were calculated and assigned to either right or left forelimbs and hindlimbs, respectively. Negative values were assigned to the left and positive values to the right limb. These measures of head and pelvic movement asymmetry are expressed as a ratio without units, as previously described (Keegan et al., 2001).
Lameness examinations and diagnostic anaesthesia All horses included in the study underwent a complete examination by a veterinarian specialising in equine lameness (JFM or LCV), including a minimum of walk and trot in a straight line and lunging in a circle in both directions on hard and soft surfaces. The primary lame limb was subjectively identified and the severity of lameness graded according to the American Association of Equine Practitioners (AAEP) scale (0–5).1 Because examination of lameness during trotting was an inclusion criterion, only horses with a forelimb lameness of grade 3 or less on the AAEP scale were included in the study. Horses were included in further analysis only if the following objective conditions for confirmation of forelimb lameness were met: (1) head movement asymmetry of greater than 0.5, and (2) maximum and/or minimum head height of >±6 mm. For all horses, the presence or absence of lameness was determined subjectively and objectively for all limbs. Hindlimb lameness was defined as a subjective AAEP lameness score of between 1 and 3 and the following objective conditions: (1) pelvic movement asymmetry of >0.17 and (2) maximum or minimum pelvic height of >±3 mm. Immediately prior to diagnostic anaesthesia each horse was trotted in a straight line on a level concrete surface with a loose lead rope to collect baseline kinematic data. Skin sensation on the distal limb was tested as part of the physical examination using a blunt probe prior to performing regional anaesthesia. Thereafter, the diagnostic anaesthesia procedure was performed as determined by the clinician (JFM or LCV). Following confirmation of desensitised by application of blunt pressure distal to the site of diagnostic anaesthesia, the horse was again trotted in a straight line (anaesthesia examination) in a similar manner to the control (baseline) examination. In cases where an intra-articular local anaesthesia block was performed the horse was trotted 10 min following the procedure. The response to the diagnostic anaesthesia was categorised by both subjective observation of improvement in gait by the clinician and also a change in objective kinematic data as previously described (Maliye et al., 2013). Briefly, a positive response was defined as: (1) a decrease in head movement asymmetry of the blocked limb to below 0.5; (2) a decrease in mean difference in maximum and/or minimum head height of >50%. Only those horses for which a positive response was confirmed both subjectively and objectively were included in the study.
Classification of lameness The primary lame limb was determined by the clinician performing the examination and horses were subsequently classified according to lameness detected in other limbs. This classification was based on the clinical scenarios of forelimb lameness only, concurrent forelimb and contralateral hindlimb lameness, and concurrent forelimb and ipsilateral hindlimb lameness. Therefore, data analysis was performed for all horses combined prior to analysis of groups consisting of (1) primary forelimb lameness only; (2) primary forelimb–contralateral hindlimb lameness, or (3) primary forelimb–ipsilateral hindlimb lameness.
Data analysis For all examinations, the vector sum of maximum and minimum head height was calculated as √([ maximum head height]2 + [ minimum head height]2) and assigned to the left or right side depending on whether minimum head height was positive or negative (Keegan et al., 2012). A Shapiro–Wilk normality test was
1 See: http://www.aaep.org/info/horse-health?publication=836 (accessed 25 February 2015).
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performed prior to data analysis. All parameters were described as median and interquartile range (IQR). The median and interquartile range of the percentage change in each parameter following diagnostic anaesthesia were calculated. Baseline measures of head and pelvic movement asymmetry were compared between groups using an ANOVA on ranks with Dunn’s post hoc test. The effect of diagnostic anaesthesia on all horses combined and within each group (forelimb-only, forelimb–contralateral hindlimb, forelimb–ipsilateral hindlimb) on all kinematic parameters was determined by Wilcoxon signed rank test. All statistical analyses were performed using commercially available software (SigmaPlot 11.2, Systat Software LLC). The correlation between the changes in measures of forelimb and hindlimb asymmetry following forelimb diagnostic anaesthesia was determined by performing Spearman’s rank correlation analysis. Correlation analysis was performed for each group (all horses, forelimb-only, forelimb–contralateral hindlimb, forelimb–ipsilateral hindlimb). Statistical significance was set at P < 0.05.
Results Medical record review A total of 28 horses with primary forelimb lameness met the inclusion criteria for this study and were grouped as follows: forelimbonly (n = 8), forelimb–contralateral hindlimb (n = 14), and forelimb– ipsilateral hindlimb (n = 6) (Table 1). Comparison of forelimb lameness between groups There was no significant difference in baseline measures of forelimb movement asymmetry between any of the groups (Table 2).
Table 1 Table describing the affected forelimb, diagnostic anaesthesia technique, and diagnosis of horses included in the study. Horse
Group
Forelimb
Diagnostic anaesthesia
Diagnosis
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
FO FO FO FO FO FO FO FO FC FC FC FC FC FC FC FC FC FC
RF RF RF LF LF LF LF RF LF LF LF RF LF RF LF LF LF RF
Palmar heel pain Pedal bone fracture Navicular disease Navicular disease DIPJ OA DDFT tear DIPJ OA DFTS synovitis Navicular disease DDFT tendonitis DDFT tendonitis DIPJ OA Unilateral laminitis Navicular disease SSL desmitis MCPJ OA DDFT tear SDFT tendonitis
19
FC
LF
20 21 22 23 24 25 26
FC FC FC FI FI FI FI
RF LF LF LF RF LF RF
27 28
FI FI
LF LF
PD PD AS AS AS AS DIPJ DFTS PD PD PD PD AS AS AS Low 4 point Low 4 point Median and ulnar nerves Median and ulnar nerves DFTS Radiocarpal joint Intercarpal joint PD PD AS Lateral palmar nerve DIPJ MCPJ
MCII osteopathy DDFT tendonitis Radiocarpal joint OA Intercarpal joint OA Navicular disease Navicular disease PIPJ OA SL desmitis DIPJ OA MCPJ OA
FO, forelimb-only lameness; FC, forelimb–contralateral hindlimb lameness; FI, forelimb–ipsilateral hindlimb lameness; LF, left forelimb; RF, right forelimb; PD, palmar digital; AS, abaxial sesamoid; DIPJ, distal interphalangeal joint; PIPJ, proximal interphalangeal joint; SDFT, superficial digital flexor tendon; DDFT, deep digital flexor tendon DDFT; DFTS, digital flexor tendon sheath; SL, suspensory ligament; SSL, straight sesamoidean ligament; MCPJ, metacarpophalangeal joint; OA, osteoarthritis.
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Table 2 The effect of diagnostic anaesthesia (blocking) of a forelimb on measures of forelimb asymmetry. Data are presented as the median and interquartile range. Group Parameter
Forelimb
Examination
All
FO
FC
FI
HMA
Blocked
Baseline Anaesthesia Baseline Anaesthesia Baseline Anaesthesia
0.84 (0.68–1.26) 0.43b (0.26–0.62) 0.02 (0.00–0.07) 0.13b (0.07–0.39) 18.25 (12.17–31.99) 5.22b (−5.36–12.15)
0.70 (0.61–1.09) 0.32a (0.01–0.583) 0.03 (0.00–0.06) 0.16a (0.11–0.67) 15.28 (12.17–27.10) −3.03a (−12.30–6.77)
1.14 (0.72–1.57) 0.54a (0.31–0.85) 0.017 (0.00–0.39) 0.11a (0.05–0.22) 30.25 (13.74–38.86) 11.61a (6.06–15.05)
0.70 (0.68–0.81) 0.33a (0.21–0.443) 0.07 (0.04–0.132) 0.39a (0.12–0.65) 14.19 (9.84–15.75) 6.78b (−13.29–4.39)
Contralateral VS (mm)
HMA, head movement asymmetry; VS, vector sum; All, all horses combined; FO, forelimb-only lameness; FC, forelimb–contralateral hindlimb lameness; FI, forelimb– ipsilateral hindlimb lameness. a Significant difference (P < 0.05) compared with baseline examination. b Significant difference (P < 0.01) compared with baseline examination.
Effect of diagnostic anaesthesia on forelimb kinematic parameters in horses with primary forelimb lameness There was a significant decrease in both the head movement asymmetry assigned to the blocked forelimb and vector sum in all of the four groups following diagnostic anaesthesia (Table 2). There was a significant increase in head movement asymmetry assigned to the contralateral forelimb in all of the four groups (Table 2). Effect of diagnostic anaesthesia on hindlimb kinematic parameters in horses with primary forelimb lameness In all horses combined and within the forelimb-only and forelimb–contralateral hindlimb groups, there was a significant decrease in the pelvic movement asymmetry assigned to the contralateral hindlimb, and a significant increase in the pelvic movement asymmetry assigned to the ipsilateral hindlimb following diagnostic anaesthesia (P < 0.05, Table 3). The contralateral hindlimb pelvic movement asymmetry decreased by a median of 38% (IQR 10–65%), 43% (IQR 28–60%) and 28% (IQR 12–67%) in all horses combined, forelimb-only and forelimb–contralateral hindlimb groups respectively. There was no significant effect of diagnostic anaesthesia on pelvic movement asymmetry of the contralateral or ipsilateral hindlimb in the forelimb–ipsilateral hindlimb group. Maximum pelvic height significantly decreased in all horses combined and within the forelimb–contralateral hindlimb group by a median of 66% (IQR 24–100%) and 78% (IQR 27–100%) respectively (P < 0.01). There was no significant effect of diagnostic anaesthesia on minimum pelvic height in any group (Table 3). Correlation analysis revealed significant positive correlations between the change in head movement asymmetry of the blocked limb and the contralateral hindlimb pelvic movement asymmetry (Figs. 1A, B) and between the change in vector sum and
the contralateral hindlimb pelvic movement asymmetry in all horses combined and within the forelimb-only and forelimb–contralateral hindlimb groups. In all horses combined and within the forelimbonly group a significant negative correlation was identified between the change in head movement asymmetry of the blocked forelimb and the pelvic movement asymmetry of the ipsilateral hindlimb and between the vector sum and the pelvic movement asymmetry of the ipsilateral hindlimb. There were significant positive correlations between the change in the head movement asymmetry of the blocked limb and the change in maximum pelvic height and the change in vector sum and the change in maximum pelvic height in all horses combined and within the forelimb-only group (Figs. 1B, C). Significant results of the correlation analysis are summarised in Table 4. Discussion The purpose of this study was to investigate compensatory load redistribution in clinical equine lameness by objectively examining the effect of reducing lameness through diagnostic anaesthesia. By measuring kinematic parameters prior to and following diagnostic anaesthesia, we have demonstrated the effect of lameness on the other limbs in horses with naturally occurring lameness under clinical examination conditions. This is in contrast to earlier studies that used experimentally-induced lameness and/or treadmill examination as a model of load re-distribution (Buchner et al., 1996a, 1996b; Uhlir et al., 1997; Kelmer et al., 2005; Weishaupt et al., 2006; Orito et al., 2007). We have demonstrated that a significant proportion of forelimb lameness cases have a concurrent compensatory lameness that is improved by diagnostic anaesthesia of the primary lame limb. Of the 28 horses included in our study, a total of 14/28 (50%) had subjective and objective evidence of forelimb and contralateral hindlimb
Table 3 The effect of diagnostic anaesthesia (blocking) of a forelimb on measures of hindlimb asymmetry. Data are presented as the median and interquartile range. Group Parameter
Hindlimb
Examination
All
FO
FC
FI
PMA
Ipsilateral
Baseline Anaesthesia Baseline Anaesthesia Baseline Anaesthesia Baseline Anaesthesia
0.06 (0.02–0.15) 0.14a (0.05–0.23) 0.18 (0.10–0.28) 0.08a (0.05–0.21) 3.62 (1.88–7.18) 1.34b (−0.63–3.65) 1.84 (0.76–5.51) 1.54 (−0.40–5.76)
0.07 (0.05–0.11) 0.15a (0.13–0.16) 0.14 (0.10–0.16) 0.07a (0.05–0.11) 1.79 (0.68–2.9) 1.34 (−1.26–2.22) 1.04 (0.67–1.48) 0.10 (−1.62–0.95)
0.02 (0.00–0.03) 0.05a (0.01–0.13) 0.28 (0.22–0.36) 0.21a (0.07–0.27) 7.18 (4.76–10.45) 1.63a (−0.23–5.22) 2.32 (0.77–5.05) 1.82 (−0.47–6.08)
0.23 (0.19–0.25) 0.26 (0.23–0.34) 0.07 (0.04–0.08) 0.02 (0.00–0.08) 2.46 (1.13–3.69) 1.03 (−5.09–2.79) 6.00 (4.26–6.56) 6.30 (3.77–7.39)
Contralateral PDMax (mm) PDMin (mm)
All, all groups combined; FO, forelimb-only lameness; FC, forelimb–contralateral hindlimb lameness; FI, forelimb–ipsilateral hindlimb lameness; PMA, pelvic movement asymmetry; PDMax, mean difference in millimetres in maximum pelvic height after the stance phases of the right and left hindlimbs; PDMin, mean difference in millimetres in minimum pelvic height during the stance phases of the right and left hindlimbs. a Significant difference (P < 0.05) compared with baseline examination. b Significant difference (P < 0.01) compared with baseline examination.
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Fig. 1. Scatter plots of the results of Spearman’s rank correlation analysis. There was a significant correlation between HMA associated with the blocked limb and PMA associated with the contralateral hindlimb in those horses with forelimb lameness only group (A, r = 0.95, P < 0.01) and horses with forelimb–contralateral hindlimb lameness (B, r = 0.68, P < 0.01). There was a significant correlation between vector sum and PDMax in all horses combined (C, r = 0.54, P < 0.01) and horses with forelimb– contralateral hindlimb lameness (D, r = 0.80, P < 0.01). HMA, measure of vertical head movement asymmetry assigned to either the right or left forelimb depending on the sign (±) of HDMin with negative values assigned to the left and positive values to the right limb. HDMax, mean difference in millimetres in maximum head height after the stance phases of the right and left forelimbs. HDMin, mean difference in millimetres in minimum head height during the stance phases of the right and left forelimb. VS, measure of head movement asymmetry, defined as √(HDMax)2 + (HDMin)2. PMA, measure of vertical head movement asymmetry assigned to either the right or left hindlimb depending on the sign (±) of PDMin with negative values assigned to the left and positive values to the right limb. PDMax, mean difference in millimetres in maximum pelvic height after the stance phases of the right and left hindlimbs. PDMin, mean difference in millimetres in minimum pelvic height during the stance phases of the right and left hindlimbs.
lameness. A total of 6/28 (21%) of horses had evidence of forelimb and ipsilateral hindlimb lameness. While the high proportion of multi-limb lameness cases reported may reflect the caseload of our referral hospital, it does illustrate the importance of identifying the primary lame limb prior to commencing lameness investigation with diagnostic anaesthesia. Similar to a previous study (Maliye et al., 2013), we found a significant effect of diagnostic anaesthesia on kinematic parameters of movement asymmetry following diagnostic anaesthesia of the lame forelimb. While the previous study was limited to horses with forelimb lameness only, our findings demonstrate the objective detection of a positive response to diagnostic anaesthesia in horses under investigation for multi-limb lameness. Moreover, we have demonstrated the objective assessment of perineural diagnostic anaesthesia proximal to the foot and intra-synovial anaesthesia. There was a significant alteration in pelvic movement asymmetry associated with both hindlimbs in all horses and both the
forelimb-only and forelimb–contralateral hindlimb lameness groups following diagnostic anaesthesia. Specifically, the pelvic movement asymmetry assigned to the contralateral hindlimb decreased while pelvic movement asymmetry assigned to the ipsilateral hindlimb increased. Furthermore, there was a significant correlation between the improvement in head movement asymmetry and improvement in pelvic movement asymmetry following diagnostic anaesthesia. A correlation between induced change in head movement and pelvic movement has been previously reported (Kelmer et al., 2005). Interestingly, the strength of the correlations was much greater in the current clinical study despite the standardised methods of the previous experimental treadmill experiment (Kelmer et al., 2005). Improvement in contralateral limb asymmetry was previously reported following diagnostic anaesthesia of forelimb lameness localised to the foot (Maliye et al., 2013). However, that study did not investigate further the reasons for this improved contralateral hindlimb asymmetry.
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Table 4 Spearman’s rank correlation analysis of the change in parameters of forelimb and hindlimb asymmetry following diagnostic anaesthesia. Spearman’s rank correlation coefficient, r, and the corresponding P values are provided for statistically significant correlations only. Group All All All All All All FO FO FO FO FC FC FC FC FI
Comparison
r value
P value
HMA (blocked limb) vs. PMA (contralateral hindlimb) HMA (blocked limb) vs. PMA (ipsilateral hindlimb) HMA (blocked limb) vs. PDMax VS vs. PMA (contralateral hindlimb) VS vs. PMA (ipsilateral hindlimb) VS vs. PDMax HMA (blocked limb) vs. PMA (contralateral hindlimb) HMA (blocked limb) vs. PMA (ipsilateral hindlimb) VS vs. PMA (contralateral hindlimb) VS vs. PMA (ipsilateral hindlimb) HMA (blocked limb) vs. PMA (contralateral hindlimb) HMA (blocked limb) vs. PDMax VS vs. PMA (contralateral hindlimb) VS vs. PDMax VS vs. PMA (contralateral hindlimb)
0.68 −0.53 0.60 0.55 −0.39 0.54 0.95 −0.86 0.71 −0.83 0.68 0.74 0.71 0.80 0.94
<0.01 <0.01 <0.01 <0.01 <0.05 <0.01 <0.01 <0.01 <0.05 <0.01 <0.01 <0.01 <0.05 <0.01 <0.05
All, all horses combined; FO, forelimb-only lameness; FC, forelimb–contralateral hindlimb lameness; FI, forelimb–ipsilateral hindlimb lameness; HMA, head movement asymmetry; VS, vector sum; PMA, pelvic movement asymmetry; PDMax, mean difference in millimetres in maximum pelvic height after the stance phases of the right and left hindlimbs; PDMin, mean difference in millimetres in minimum pelvic height during the stance phases of the right and left hindlimbs.
Our study demonstrated that in clinical cases of forelimb lameness there was a significant decrease in the difference in maximum pelvic height after the stance phase of the left and right hindlimbs associated with a positive response to diagnostic anaesthesia. Furthermore, in all horses with forelimb lameness and among those with concurrent contralateral hindlimb lameness there was a significant correlation between the change in measures of forelimb asymmetry and the difference in maximum pelvic height after the stance phase of the left and right hindlimbs i.e. push-off. This implies that compensatory lameness or load re-distribution in these groups is associated with the push-off component of the stride rather than impact and loading. Specifically, forelimb lameness resulted in a decrease in push-off from the contralateral hindlimb that was improved by diagnostic anaesthesia. Previous experimental studies have demonstrated a shift in loading from the lame forelimb to the diagonal hindlimb (Vorstenbosch et al., 1997; Weishaupt et al., 2006). In the present study, diagnostic anaesthesia resulted in a significant increase in loading of the forelimb (decreased vector sum) that was significantly correlated with an increase in push-off (decreased difference in maximum pelvic height after stance phase of hindlimbs) from the contralateral hindlimb. Therefore, the reduction in hindlimb push-off associated with forelimb lameness is most likely a reflection of increased loading of the hindlimb. Previous studies have disagreed about whether forelimb lameness results in a compensatory weight-bearing ipsilateral hindlimb lameness (Weishaupt et al., 2006), or a contralateral hindlimb lameness (Uhlir et al., 1997) using ground-reaction force measurement and kinematics, respectively. There was no significant change in the difference in minimum pelvic height during stance phase between the left and right hindlimbs following diagnostic anaesthesia, nor a correlation between minimum pelvic height and either of the measures of forelimb asymmetry in any group. In addition, pelvic movement asymmetry associated with the ipsilateral hindlimb was actually observed to increase significantly following diagnostic anaesthesia in all groups except those horses with forelimb lameness and ipsilateral hindlimb lameness. We were therefore unable to identify evidence of compensatory ipsilateral weight-bearing lameness in this population of horses. The current study of naturally occurring lameness during a clinical examination suggests that a reduction in push-off from the contralateral hindlimb in cases of forelimb
lameness can result in perceived false or compensatory contralateral hindlimb lameness. In the current study, the purpose of analysing the horses as subgroups was to investigate the specific clinical scenarios encountered during lameness investigation. Although there was a significant effect of diagnostic anaesthesia on the forelimb lameness, there was no significant change in any of the measured hindlimb kinematic parameters in the group of horses with concurrent ipsilateral hindlimb lameness. These findings, in combination with the lack of improvement in ipsilateral lameness when all horses were analysed, suggest that the lameness in the ipsilateral hindlimb of these horses was a ‘true’ lameness and not the result of compensatory load distribution. However, this difference may also reflect the differences in experimental methods including the use of inertial sensors rather than a camera based kinematic system, data analysis and horse populations between previous studies and our study. In the current study, the concurrent ipsilateral hindlimb lameness group was the smallest with six horses. This will have reduced the statistical power of the analysis to identify a significant difference in hindlimb parameters. Therefore, a further analysis of a larger group of horses is warranted. The low number of horses reflects the clinical nature of the population as the clinicians involved in this study generally performed diagnostic anaesthesia in the hindlimb of horses with ipsilateral forelimb and hindlimb lameness. Overall, the analysis of forelimb diagnostic anaesthesia provides significant clinical evidence that forelimb lameness results in significant compensatory load distribution that is manifest as contralateral hindlimb lameness. Furthermore, while a previous study found evidence of compensatory contralateral limb lameness in horses with severe forelimb lameness (Uhlir et al., 1997), we have demonstrated detectable and significant load redistribution in horses with mild or moderate forelimb lameness and both with and without observed hindlimb lameness. Conclusions Our study has expanded upon previously assumed knowledge by characterising the compensatory hindlimb lameness associated with primary forelimb lameness. By objectively examining this population of horses with clinical lameness we have provided strong evidence objectively supporting part of the ‘law of sides’. When assessing the lame horse it is important to eliminate hindlimb lameness as a possible cause of forelimb lameness and vice versa prior to performing further diagnostic techniques. In addition, when assessing the response to diagnostic anaesthesia in horses with forelimb and hindlimb lameness it is useful to define the effect on both the hind and forelimb movements. Conflict of interest statement None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper. Acknowledgements We wish to thank everyone who was involved with helping during lameness examinations undertaken at the Weipers Centre, University of Glasgow. References Buchner, H.H., Savelberg, H.H., Schamhardt, H.C., Barneveld, A., 1996a. Head and trunk movement adaptations in horses with experimentally induced fore- or hindlimb lameness. Equine Veterinary Journal 28, 71–76.
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