Accepted Manuscript Comparison of superficial digital flexor tendon loading on asphalt and sand in horses at the walk and trot N. Crevier-Denoix, B. Ravary-Plumioen, C. Vergari, M. Camus, L. HoldenDouilly, S. Falala, H. Jerbi, L. Desquilbet, H. Chateau, J.-M. Denoix, P. Pourcelot PII: DOI: Reference:
S1090-0233(13)00475-9 http://dx.doi.org/10.1016/j.tvjl.2013.09.047 YTVJL 3903
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The Veterinary Journal
Please cite this article as: Crevier-Denoix, N., Ravary-Plumioen, B., Vergari, C., Camus, M., Holden-Douilly, L., Falala, S., Jerbi, H., Desquilbet, L., Chateau, H., Denoix, J.-M., Pourcelot, P., Comparison of superficial digital flexor tendon loading on asphalt and sand in horses at the walk and trot, The Veterinary Journal (2013), doi: http:// dx.doi.org/10.1016/j.tvjl.2013.09.047
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Comparison of superficial digital flexor tendon loading on asphalt and sand in horses at the walk and trot N. Crevier-Denoix a,b,*, B. Ravary-Plumioen a,b, C. Vergari a,b, M. Camus a,b, L. HoldenDouilly a,b, S. Falala a,b, H. Jerbi c, L. Desquilbet d, H. Chateau a,b, J.-M. Denoix a,e, P. Pourcelot a,b a
Université Paris Est, Ecole Nationale Vétérinaire d’Alfort, USC 957 BPLC, F-94700 Maisons-Alfort, France b INRA, USC 957 BPLC, F-94700 Maisons-Alfort, France c Service d'Anatomie, Ecole Nationale de Médecine Vétérinaire de Sidi Thabet, CP 202, Tunisie d Université Paris Est, Ecole Nationale Vétérinaire d’Alfort, USC EpiMAI, F-94700 MaisonsAlfort, France e Université Paris Est, Ecole Nationale Vétérinaire d’Alfort, CIRALE, F-14430 Goustranville, France
* Corresponding author. Tel.: + 33 1 43967106. E-mail address: [email protected] (N. Crevier-Denoix).
Abstract The incidence of superficial digital flexor tendon (SDFT) injuries is one of the highest of all equine musculoskeletal conditions. Horses with SDFT injuries commonly show no improvement of lameness on soft ground, unlike those suffering from distal bone or joint lesions. The aim of this study was to compare the SDFT loading in five horses at the walk and trot on asphalt and sand using a non-invasive ultrasonic tendon force measurement device. Three horses were equipped with the ultrasonic device, whereas the other two horses were equipped with the ultrasonic device and a dynamometric horseshoe (DHS); the DHS was used to calibrate the measured values of tendon speed of sound (SOS) converted to tendon force, while a previously established ground reaction force pattern was used to calibrate SOS measurements for the other three horses. Although the horses tended to be slower on S, maximal tendon force was higher on sand than on asphalt at the trot (+6%); there was no significant difference between the two surfaces at the walk. The duration of tendon loading was longer on S (+5%) and the area under the tendon force-time curve was larger on S (+10%) at both walk and trot. SDFT loading is significantly affected by the ground surface and the observed increase in SDFT loading on sand compared with asphalt is consistent with clinical observations in horses with SDFT injuries.
Keywords: Equine; Ground surface; Speed of sound; Tendon force; Superficial digital flexor tendon
Introduction Superficial digital flexor tendon (SDFT) injuries are amongst the most common lesions in race and sport horses (Denoix, 1995; Williams et al., 2001; Ely et al., 2004; Lam et al., 2007). Their economic impact may be the highest of all musculoskeletal conditions, especially in racehorses, where these injuries often recur (Marr et al., 1993; Dyson, 2004). Affected horses commonly do not show improvement of lameness on soft ground, unlike those suffering from distal bone or joint lesions (Denoix, 1992, 1995; Ross, 2011). However, to date no study has elucidated the reasons for this clinical aspect of SDFT injuries and no study has demonstrated a significant effect of soft vs. firm ground on SDFT loading.
Riemersma et al. (1996b) implanted strain gauges in the four palmar tendon structures of the distal forelimb (SDFT, deep digital flexor tendon (DDFT) and its accessory ligament (AL-DDFT), and the third interosseous muscle (or suspensory ligament, SL) of five ponies and compared tendon loading at the walk and trot on asphalt and on a loose sand track. At the walk, there was a significant increase in the maximal strain on the DDFT and the AL-DDFT, and (except for one pony) a significant decrease in the maximal strain on the SL on asphalt compared with sand, but no significant difference was observed in the SDFT. At the trot, the maximal strain of the AL-DDFT and SL (both passive structures) was significantly increased on asphalt compared with sand; although the same tendency was observed in both flexor tendons, the difference between surfaces was non-significant. These results, obtained in ponies with an invasive device, cannot explain the clinical observation that the lameness of horses (most often examined at the trot) suffering from a SDFT injury usually is not improved on soft ground.
In vivo investigations on equine tendon loading have remained limited, since only
invasive techniques were available until the last decade (Ravary et al., 2004). A non-invasive ultrasonic technique, based on the measurement of speed of sound (SOS) in the tendon (Pourcelot et al., 2005) has been applied to the measurement of SDFT loading in French trotters on two training surfaces (Crevier-Denoix et al., 2009a). Since SOS in a tendon is mainly influenced by the tendon’s material properties, especially its elastic modulus (Vergari et al., 2012a), the SOS value at a given tendon force may vary between tendons. However intra-individual reproducibility of SOS measurements has been demonstrated in vivo in horses at the walk and trot (Ravary 2005), and reproducibility of the SOS-force relationship in a given tendon has been established in vitro (Crevier-Denoix et al., 2009b).
Under some assumptions, it is possible to calibrate SOS measures (expressed in m/s) determined for a given tendon in terms of force (expressed in N) to compare tendon loading under different exercise conditions. The calibration procedure requires the simultaneous measurement of the ground reaction force (GRF); however, when no dynamometric device is available, a previously established GRF pattern (Merkens et al., 1993) can be used as an alternative (Vergari et al., 2012b).
Using the ultrasonic technique and both types of calibration procedure, the aim of the present study was to compare the equine SDFT loading in horses walking and trotting on asphalt and on sand. Given the clinical observations, the hypothesis tested was that soft ground would not induce a decrease of the SDFT loading compared with asphalt.
Materials and methods Horses Five French trotters (2 geldings, 3 females; mean ± standard deviation, SD, body mass
557 ± 32 kg; age 8 ± 4 years) were used in this study. All horses were clinically sound, with no subjectively observed gait abnormality. The local Animal Care and Ethics Committee advised that no formal approval was required for this study.
Experimental set-up The right palmar metacarpal region of each horse was depilated then equipped with an ultrasonic probe facing the SDFT by means of an adapted boot (Fig. 1). The probe, composed of three transducers (1 MHz; one acting as an emitter, the other two as receivers), was connected to an electronic module placed on a saddle. Each horse was led in hand, at the walk and at the trot, along two 30 m long tracks, one asphalt surface and one sand and fibre mix surface (sand). Ultrasonic recordings (8 s, 100 Hz) were repeated 3-6 times at each gait on each surface in a random sequence. From each trial (ultrasonic recording), 6-10 successive strides were analysed.
Three horses (group 1) were equipped only with the US device, whereas the right forehoof of the other two horses (group 2) was also equipped with a 3-dimensional dynamometric horseshoe (DHS). The latter was composed of four triaxial piezoelectric force sensors (model 9251A, Kistler) sandwiched between two aluminium plates (Chateau et al., 2009; Fig. 1). A non-instrumented horseshoe with matching height and weight was attached to the left front hoof of these two horses. The recordings of the DHS (sampled at 7800 Hz, then resampled at 100 Hz) were synchronised with the US data. All electronics and portable computers for synchronous acquisition were carried in bags placed behind or on the saddle and remotely controlled via WiFi (UltraVNC Free Software Foundation).
The horses’ speed was maintained as similar as possible on both surfaces (each horse
being led by the same operator on both surfaces); speed was estimated by dividing the known distance between two landmarks placed at the beginning and end of each track by the time (measured with a stopwatch) taken by the horse walking or trotting from one landmark to the other.
Data processing The speed of sound (SOS) was measured as the speed of the first arriving signal (Pourcelot et al. 2005), then converted to tendon force following two different procedures. In group 2, a tendon SOS-force calibration relationship was determined for each horse using the SOS data measured at the trot on asphalt (in all the corresponding trials) and the simultaneously recorded vertical component of the GRF (GRFz) measured by the DHS. On the basis of the linear relationship demonstrated by Jerbi et al. (2000) between the SDFT tensile force and the limb vertical compression force on isolated forelimbs vertically compressed in a mid-stance attitude (average ratio between both forces 0.76 ± 0.13), the measured GRFz was multiplied by 0.76 to obtain the SDFT force. The SDFT SOS-force relationship around mid-stance (i.e. 25-70 % of stance; Vergari et al., 2012b) was approximated with a logarithm (Pourcelot et al., 2005), the inverse of which was then used to convert SOS data of all trials of that particular horse to force values.
In group 1, since no dynamometric device was available, the measured GRFz was replaced by the average values of GRFz (measured with a force plate and normalised to body mass) reported by Merkens et al. (1993) for horses trotting on a firm flat surface. The GRFz graph reported by these authors was digitised then interpolated. For each horse, the relationship between the GRFz thus evaluated (adapted to each horse’s body mass) and the SOS measured in all trials at the trot on asphalt was approximated to 25-70 % of stance with a
logarithm. The inverse of this logarithm was used to convert SOS data of all trials of this horse to force values.
Stride duration was also measured. In horses from group 1, hoof contact was identified via a characteristic event on the SOS chart (correspondence of this event with hoof contact was confirmed in horses in group 2 using the simultaneous DHS measurements). In group 2, stride duration was measured directly from the GRFz.
For both groups, the maximal tendon force and corresponding time, the duration of tendon loading and the area under the tendon force-time curve were determined. The duration of tendon loading was calculated as the time during which the tendon force was > 100 N (which represents ~3% of maximal tendon force at the walk and 2% at the trot); this threshold was also used for the calculation of the area under the tendon force-time curve.
Statistical analysis To compare the effects of the two surfaces on the parameters studied and to adjust for repeated measurements within each horse, linear mixed-effects regression models were used (SAS version 9.2). Results were considered to be significant when P values were < 0.05.
Results The five horses were significantly slower on sand than asphalt, both at the walk (speed mean ± SD: sand 1.58 ± 0.14 m/s; asphalt 1.61 ± 0.12 m/s; P = 0.0478) and at the trot (sand 3.12 ± 0.36 m/s; asphalt 3.41 ± 0.46 m/s; P < 0.0001). As a consequence, stride duration was longer on sand than asphalt (P = 0.0008 at the walk; P < 0.0001 at the trot; Table 1). The average tendon force-time curves of each horse on both surfaces are presented in Figs. 2A and
2B. At the walk, the tendon force-time curve typically showed two peaks, the first one always being the highest, whereas a single peak was present at the trot. Although this general shape was observed in all horses, inter-individual variations in the SDFT loading pattern were apparent at both gaits.
Although there was a lower speed on sand, the maximal tendon force was higher on this surface than on asphalt at the trot (+6%; P = 0.037); at the walk, there was no significant difference between sand and asphalt at the first or second peaks (Table 1). The time of maximal tendon force was delayed on sand at both gaits (and for both peaks at the walk), when expressed in seconds (+9% in average; P < 0.0001 in all cases); when time was expressed in % of stride duration, the difference between surfaces was significant only at the walk (P < 0.0001 for both peaks). The duration of tendon loading was longer on sand (mean +5% when expressed in seconds and +2% when expressed as % of stride duration; P < 0.001 in all cases except at the trot when expressed in % of stride duration, where P = 0.060). The area under the tendon force-time curve was larger on sand (+10% in average), both at the walk (P = 0.043) and trot (P < 0.0001).
Figs. 3A and 3B show the average vertical component of the GRF (GRFz) measured with the DHS vs. time, for the two horses in group 2. Both GRFz peaks were lower on sand than asphalt at the walk (mean ± SD: first peak on asphalt 3434.8 ± 294.4 N vs. sand 3312.1 ± 204.7 N, P = 0.013; second peak on asphalt 3715.1 ± 357.7 N vs. sand 3652.3 ± 345.0 N, P = 0.016) and the single peak at the trot (asphalt 5901.4 ± 226.1 N vs. sand 5771.0 ± 230.8 N, P = 0.001).
Discussion
Significant differences in loading of the equine SDFT on a soft ground surface compared with an asphalt surface were demonstrated in this study using the non-invasive ultrasonic technique. SDFT force values were obtained after calibration of the SOS values directly measured with the device. In both groups of horses, the calibration procedure was based on the linear relationship previously demonstrated in vitro between the force applied to forelimbs vertically compressed in a standing position and the corresponding SDFT force (Jerbi et al., 2000). This relationship was determined by combining limb compression tests (on four left forelimbs isolated at the distal third of the humerus) with SDFT traction tests (isolated from the same limbs). The four horses used in the study of Jerbi et al. (2000) had characteristics (mean body mass 557 ± 83 kg; mean age 8.8 ± 1.7 years) similar to those of the five horses in the present study, although the breed of horse was different; Jerbi et al. (2000) used French Warmbloods, whereas the present study used French trotters.
Using a unique ratio (0.76) to convert limb compression force (or GRFz) to SDFT force may lead to systematic errors in the tendon force calculation in a given horse, since this ratio is likely to be dependent on the conformation of each horse and on the structural and material properties of the SDFT. Furthermore, this ratio was determined in vitro, neglecting the participation of the SDF muscle and assuming that distal limb kinematics during compression tests are the same as in vivo during mid-stance, which is likely to be an oversimplification. However, it should be noted that Takahashi et al. (2010), combining the use of an arthroscopically implantable force probe in the SDFT and force plate measurements in seven thoroughbreds at the trot (3 m/s), found a ratio of maximum SDFT force to maximum GRFz of 0.82 ± 0.24, which is similar to the value used here.
Taking into account the variability of the ratio (0.76 ± 2 SD), it can be demonstrated that the difference (in N) in the SDFT force between sand and asphalt varies by ± 34%. In other words, a difference of 100 N between sand and asphalt with a 0.76 ratio would become 66 N with a 0.5 ratio and 134 N with a 1.02 ratio. However, the ratio value has no impact on the relative difference between surfaces (i.e. when the force difference is divided by the SDFT force on asphalt) and thus no effect on the average increase of 6-7 % in the SDFT peak force observed here on sand compared with asphalt. Furthermore, the ratio has no impact on the SDFT loading pattern. Thus, the inter-individual variations in the SDFT loading pattern apparent in the present study, both at the walk and trot, which confirm previous observations made from invasive measurements (Jansen et al., 1993), would not be affected if a subjectspecific ratio had been used.
Calibration of SOS measurements using the GRFz pattern previously established on another equine population, instead of the simultaneously measured vertical force from the same horse, also introduces an error, as discussed by Vergari et al. (2012b). In the present study, using the previously established GRF pattern in group 2 horses would lead to an overestimation of the SDFT peak force difference between the two surfaces by 8% on average at the walk and trot (i.e. a difference of 6% between sand and asphalt, when measured using the DHS, would become 6.5%).
Although the values of SDFT force obtained in the present study are affected by the approximations and errors mentioned above, these values are consistent with those obtained in horses using invasive devices, both at the walk and trot (Lochner et al., 1980; Butcher et al., 2007; Takahashi et al., 2010). Furthermore, since the same relation was applied to all trials of a given horse, under the assumption that the SDFT SOS-force relationship is
reproducible in a given tendon (Crevier-Denoix et al., 2009b), the calibration procedures used here should not affect the comparison between surfaces.
The present study demonstrated an overall increase in SDFT loading on sand compared with asphalt; the duration of tendon loading and the area under the tendon forcetime curve were significantly increased on sand, both at the walk and trot, and tendon maximal force was significantly higher on sand at the trot. This SDFT loading increase was observed even though the horses were generally slower on sand and (in the two DHS equipped horses) while the simultaneously measured GRFz was decreased on sand.
The increased stride duration measured on sand has also been described by Riemersma et al. (1996b) in ponies (weighing 165-240 kg) on a loose sand track compared with pavement. Although no significant effect of ground surface type on the selected SDFT loading parameters could be demonstrated by Riemersma et al. (1996b), the tendon strain charts presented by these authors are similar to those of our study; the SDFT loading (expressed as SDFT strain) duration was increased on sand both at the walk and trot, as was the second peak of SDFT strain at the walk and, to a lesser extent, the single peak at the trot. Times of maximal strain (in % of stride duration) were also delayed, as in the present study. The absence of a significant difference between types of ground surface at the walk can be explained by the fact that Riemersma et al. (1996b) only considered the maximal SDFT strain, i.e. only the first peak of the curve, for which no significant difference was observed in the present study, contrary to the second peak.
The absence of a significant difference in strain on the SDFT between types of ground surface obtained by Riemersma et al. (1996b), although somewhat in contradiction with the
presented charts, could be explained by the distal limb conformation of ponies. Ponies have small feet, with relatively high heels and a short toe, which implies a reduced lever arm of the GRF acting on the distal interphalangeal joint. Furthermore, ponies have a less ample propulsion phase of the stance compared with horses, which minimises the digital joint angle changes observed during this phase. Maximal SDFT forces measured by Riemersma et al. (1996b) in ponies at the walk (~2.2-2.6 N) and slow trot (~6.7 N/kg) were lower than those obtained in horses (~6-7 N/kg at the walk; 8.5-11 N/kg at the trot) in the present study and by other authors (Lochner et al., 1980; Butcher et al., 2007; Takahashi et al., 2010; Vergari et al., 2012b). This may also have a link with the more subtle effects on the SDFT recorded in ponies (vs. horses) when changing ground surface or hoof angle (Riemersma et al., 1996a and b).
Riemersma et al. (1996b) measured the angle between the sole of the hoof and the ground surface at the walk on sand and demonstrated a small positive caudal angle, i.e. a hoof orientation similar to an elevation of the heels. In all ponies, this heel elevation hoof orientation increased during the stance phase by 4.8-12.6 °. Compared with the situation on asphalt, where the hoof cannot penetrate the ground surface, this forward rotation on sand implies an increased distal interphalangeal flexion, which has been confirmed by kinematic studies (Scheffer and Back, 2001). Since distal interphalangeal joint flexion provokes DDFT release, this movement is accompanied by dropping of the fetlock (extension), as demonstrated in standing horses (Denoix, 1985; Crevier-Denoix et al., 2001) and horses at the walk (Chateau et al., 2004); this in turn increases SDFT and SL loading (Denoix, 1994). Active contraction of the flexor muscles at the end of stance (propulsion phase), which is necessarily increased on a soft, less reactive, ground than on a firm surface, is also expected to increase the SDFT loading further.
It is now established that firmer surfaces are a risk factor for SDFT injuries in race horses (Williams et al., 2001; Reardon et al., 2012), probably because of an increased SDFT loading rate at high speed. The results of the present study nevertheless demonstrate the rationale of rehabilitating SDFT injuries on firm ground surfaces at slow gaits.
Conclusions The results of this study demonstrate that the SDFT loading is significantly affected by ground surface, with increased loading on sand compared with asphalt. The combined increases in maximal SDFT force, duration of tendon loading and area under the tendon force-time curve during stance observed in the present study are consistent with the clinical observations that horses suffering from SDFT injuries generally do not show improvement of their lameness when examined on soft ground.
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 The authors thank the Conseil Régional de Basse-Normandie, the Fonds Unique Interministériel, the French Ministry of Agriculture, the Fonds Européen de Développement Régional (FEDER) and the Institut Français du Cheval et de l’Equitation (IFCE) for their financial support for this project. We are very grateful to Fabrice Cavé and Jean-Michel Goubault, farriers (IFCE), as well as Elodie Paumier-André, technician (CIRALE), for their participation, and to the CIRALE and IFCE for loaning horses. The authors also thank
Romuald Glowacki and the Pôle de Compétitivité Hippolia for their logistical and administrative support, as well as Guy Launay for assistance with the manuscript.
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Table 1 Mean and standard deviation (SD) of stride duration and superficial digital flexor tendon loading variables measured in five horses at the walk and trot alternately on asphalt and on a sand and fibre mix (sand) surface.
Stride duration (s) Maximal tendon force (walk first peak) (N) Maximal tendon force (walk second peak) (N) Time of maximal tendon force (walk first peak) (s) Time of maximal tendon force (walk second peak) (s) Time of maximal tendon force (walk first peak) (% of stride duration) Time of maximal tendon force (walk second peak) (% of stride duration) Duration of tendon loading (s) Duration of tendon loading (% of stride duration) Area under the tendon-force time curve (Ns)
* Significant differences between surfaces: P < 0.05.
Asphalt (n = 117) Mean SD 1.156 0.053 3517.6 480.1 2076.0 629.8 0.158 0.018 0.422 0.046 13.9 1.6 36.7 3.7 0.613 0.072 52.9 4.4 1172.7 201.7
Walk Sand (n = 121) Mean SD 1.178 0.057 3609.7 548.8 2216.8 573.3 0.179 0.026 0.455 0.042 15.6 2.2 38.9 4.0 0.641 0.073 54.4 4.5 1278.6 223.4
Trot
P* < 0.01 0.5 0.1 < 0.01 < 0.01 < 0.01 < 0.01 < 0.01 < 0.01 < 0.05
Asphalt (n = 182) Mean SD 0.717 0.043 4715.6 572.0
Sand (n = 156) Mean SD 0.749 0.043 4976.3 339.8
P* < 0.01 < 0.05
0.150
0.019
0.159
0.023
< 0.01
21.0
2.3
21.3
2.9
0.2
0.259 36.0 820.7
0.031 2.8 133.8
0.274 36.4 907.5
0.036 3.2 133.8
< 0.01 0.06 < 0.01
Figure legends
Fig. 1. Experimental device to study the effects of ground surface on the superficial digital flexor tendon loading in horses at the walk and trot. The right forelimb of each horse is equipped with an ultrasonic probe (1 MHz) facing the palmar metacarpal area. The probe, covered with acoustic gel, is inserted in an adapted (windowed) tendon boot and placed in contact with the skin (A). The probe in the boot is maintained by an elastic band and connected to an electronic module placed on the saddle. In two horses, the right forehoof was also equipped with a dynamometric horseshoe composed of four triaxial piezoelectric force sensors (B); the vertical component of the ground reaction force (GRFz) was directed proximo-distally (perpendicular to the plane of the shoe). The corresponding electronic devices are placed in saddle-bags. A WiFi-connection is used to acquire data remotely.
Fig. 2. Force in the superficial digital flexor tendon of the right forelimbs of five horses at the walk (A) and trot (B) on asphalt (dark grey) and on a sand and fibre mix (sand) surface (light grey) during averaged strides (n = 19-34 strides per horse on each surface at the walk; n = 2157 strides per horse at the trot). The time bases are standardised to a complete stride.
Fig. 3. Vertical component of the ground reaction force (GRFz) measured with a dynamometric horseshoe placed on the right forehoof of two horses at the walk (A) and at the trot (B) on asphalt (dark grey) and on a sand and fibre mix (sand) surface (light grey) during averaged strides (n = 24-34 strides per horse on each surface at the walk; n = 44-57 strides per horse at the trot). The time bases are standardised to a complete stride.
S1090-0233(13)00475-9 http://dx.doi.org/10.1016/j.tvjl.2013.09.047 YTVJL 3903
To appear in:
The Veterinary Journal
Please cite this article as: Crevier-Denoix, N., Ravary-Plumioen, B., Vergari, C., Camus, M., Holden-Douilly, L., Falala, S., Jerbi, H., Desquilbet, L., Chateau, H., Denoix, J.-M., Pourcelot, P., Comparison of superficial digital flexor tendon loading on asphalt and sand in horses at the walk and trot, The Veterinary Journal (2013), doi: http:// dx.doi.org/10.1016/j.tvjl.2013.09.047
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Comparison of superficial digital flexor tendon loading on asphalt and sand in horses at the walk and trot N. Crevier-Denoix a,b,*, B. Ravary-Plumioen a,b, C. Vergari a,b, M. Camus a,b, L. HoldenDouilly a,b, S. Falala a,b, H. Jerbi c, L. Desquilbet d, H. Chateau a,b, J.-M. Denoix a,e, P. Pourcelot a,b a
Université Paris Est, Ecole Nationale Vétérinaire d’Alfort, USC 957 BPLC, F-94700 Maisons-Alfort, France b INRA, USC 957 BPLC, F-94700 Maisons-Alfort, France c Service d'Anatomie, Ecole Nationale de Médecine Vétérinaire de Sidi Thabet, CP 202, Tunisie d Université Paris Est, Ecole Nationale Vétérinaire d’Alfort, USC EpiMAI, F-94700 MaisonsAlfort, France e Université Paris Est, Ecole Nationale Vétérinaire d’Alfort, CIRALE, F-14430 Goustranville, France
* Corresponding author. Tel.: + 33 1 43967106. E-mail address: [email protected] (N. Crevier-Denoix).
Abstract The incidence of superficial digital flexor tendon (SDFT) injuries is one of the highest of all equine musculoskeletal conditions. Horses with SDFT injuries commonly show no improvement of lameness on soft ground, unlike those suffering from distal bone or joint lesions. The aim of this study was to compare the SDFT loading in five horses at the walk and trot on asphalt and sand using a non-invasive ultrasonic tendon force measurement device. Three horses were equipped with the ultrasonic device, whereas the other two horses were equipped with the ultrasonic device and a dynamometric horseshoe (DHS); the DHS was used to calibrate the measured values of tendon speed of sound (SOS) converted to tendon force, while a previously established ground reaction force pattern was used to calibrate SOS measurements for the other three horses. Although the horses tended to be slower on S, maximal tendon force was higher on sand than on asphalt at the trot (+6%); there was no significant difference between the two surfaces at the walk. The duration of tendon loading was longer on S (+5%) and the area under the tendon force-time curve was larger on S (+10%) at both walk and trot. SDFT loading is significantly affected by the ground surface and the observed increase in SDFT loading on sand compared with asphalt is consistent with clinical observations in horses with SDFT injuries.
Keywords: Equine; Ground surface; Speed of sound; Tendon force; Superficial digital flexor tendon
Introduction Superficial digital flexor tendon (SDFT) injuries are amongst the most common lesions in race and sport horses (Denoix, 1995; Williams et al., 2001; Ely et al., 2004; Lam et al., 2007). Their economic impact may be the highest of all musculoskeletal conditions, especially in racehorses, where these injuries often recur (Marr et al., 1993; Dyson, 2004). Affected horses commonly do not show improvement of lameness on soft ground, unlike those suffering from distal bone or joint lesions (Denoix, 1992, 1995; Ross, 2011). However, to date no study has elucidated the reasons for this clinical aspect of SDFT injuries and no study has demonstrated a significant effect of soft vs. firm ground on SDFT loading.
Riemersma et al. (1996b) implanted strain gauges in the four palmar tendon structures of the distal forelimb (SDFT, deep digital flexor tendon (DDFT) and its accessory ligament (AL-DDFT), and the third interosseous muscle (or suspensory ligament, SL) of five ponies and compared tendon loading at the walk and trot on asphalt and on a loose sand track. At the walk, there was a significant increase in the maximal strain on the DDFT and the AL-DDFT, and (except for one pony) a significant decrease in the maximal strain on the SL on asphalt compared with sand, but no significant difference was observed in the SDFT. At the trot, the maximal strain of the AL-DDFT and SL (both passive structures) was significantly increased on asphalt compared with sand; although the same tendency was observed in both flexor tendons, the difference between surfaces was non-significant. These results, obtained in ponies with an invasive device, cannot explain the clinical observation that the lameness of horses (most often examined at the trot) suffering from a SDFT injury usually is not improved on soft ground.
In vivo investigations on equine tendon loading have remained limited, since only
invasive techniques were available until the last decade (Ravary et al., 2004). A non-invasive ultrasonic technique, based on the measurement of speed of sound (SOS) in the tendon (Pourcelot et al., 2005) has been applied to the measurement of SDFT loading in French trotters on two training surfaces (Crevier-Denoix et al., 2009a). Since SOS in a tendon is mainly influenced by the tendon’s material properties, especially its elastic modulus (Vergari et al., 2012a), the SOS value at a given tendon force may vary between tendons. However intra-individual reproducibility of SOS measurements has been demonstrated in vivo in horses at the walk and trot (Ravary 2005), and reproducibility of the SOS-force relationship in a given tendon has been established in vitro (Crevier-Denoix et al., 2009b).
Under some assumptions, it is possible to calibrate SOS measures (expressed in m/s) determined for a given tendon in terms of force (expressed in N) to compare tendon loading under different exercise conditions. The calibration procedure requires the simultaneous measurement of the ground reaction force (GRF); however, when no dynamometric device is available, a previously established GRF pattern (Merkens et al., 1993) can be used as an alternative (Vergari et al., 2012b).
Using the ultrasonic technique and both types of calibration procedure, the aim of the present study was to compare the equine SDFT loading in horses walking and trotting on asphalt and on sand. Given the clinical observations, the hypothesis tested was that soft ground would not induce a decrease of the SDFT loading compared with asphalt.
Materials and methods Horses Five French trotters (2 geldings, 3 females; mean ± standard deviation, SD, body mass
557 ± 32 kg; age 8 ± 4 years) were used in this study. All horses were clinically sound, with no subjectively observed gait abnormality. The local Animal Care and Ethics Committee advised that no formal approval was required for this study.
Experimental set-up The right palmar metacarpal region of each horse was depilated then equipped with an ultrasonic probe facing the SDFT by means of an adapted boot (Fig. 1). The probe, composed of three transducers (1 MHz; one acting as an emitter, the other two as receivers), was connected to an electronic module placed on a saddle. Each horse was led in hand, at the walk and at the trot, along two 30 m long tracks, one asphalt surface and one sand and fibre mix surface (sand). Ultrasonic recordings (8 s, 100 Hz) were repeated 3-6 times at each gait on each surface in a random sequence. From each trial (ultrasonic recording), 6-10 successive strides were analysed.
Three horses (group 1) were equipped only with the US device, whereas the right forehoof of the other two horses (group 2) was also equipped with a 3-dimensional dynamometric horseshoe (DHS). The latter was composed of four triaxial piezoelectric force sensors (model 9251A, Kistler) sandwiched between two aluminium plates (Chateau et al., 2009; Fig. 1). A non-instrumented horseshoe with matching height and weight was attached to the left front hoof of these two horses. The recordings of the DHS (sampled at 7800 Hz, then resampled at 100 Hz) were synchronised with the US data. All electronics and portable computers for synchronous acquisition were carried in bags placed behind or on the saddle and remotely controlled via WiFi (UltraVNC Free Software Foundation).
The horses’ speed was maintained as similar as possible on both surfaces (each horse
being led by the same operator on both surfaces); speed was estimated by dividing the known distance between two landmarks placed at the beginning and end of each track by the time (measured with a stopwatch) taken by the horse walking or trotting from one landmark to the other.
Data processing The speed of sound (SOS) was measured as the speed of the first arriving signal (Pourcelot et al. 2005), then converted to tendon force following two different procedures. In group 2, a tendon SOS-force calibration relationship was determined for each horse using the SOS data measured at the trot on asphalt (in all the corresponding trials) and the simultaneously recorded vertical component of the GRF (GRFz) measured by the DHS. On the basis of the linear relationship demonstrated by Jerbi et al. (2000) between the SDFT tensile force and the limb vertical compression force on isolated forelimbs vertically compressed in a mid-stance attitude (average ratio between both forces 0.76 ± 0.13), the measured GRFz was multiplied by 0.76 to obtain the SDFT force. The SDFT SOS-force relationship around mid-stance (i.e. 25-70 % of stance; Vergari et al., 2012b) was approximated with a logarithm (Pourcelot et al., 2005), the inverse of which was then used to convert SOS data of all trials of that particular horse to force values.
In group 1, since no dynamometric device was available, the measured GRFz was replaced by the average values of GRFz (measured with a force plate and normalised to body mass) reported by Merkens et al. (1993) for horses trotting on a firm flat surface. The GRFz graph reported by these authors was digitised then interpolated. For each horse, the relationship between the GRFz thus evaluated (adapted to each horse’s body mass) and the SOS measured in all trials at the trot on asphalt was approximated to 25-70 % of stance with a
logarithm. The inverse of this logarithm was used to convert SOS data of all trials of this horse to force values.
Stride duration was also measured. In horses from group 1, hoof contact was identified via a characteristic event on the SOS chart (correspondence of this event with hoof contact was confirmed in horses in group 2 using the simultaneous DHS measurements). In group 2, stride duration was measured directly from the GRFz.
For both groups, the maximal tendon force and corresponding time, the duration of tendon loading and the area under the tendon force-time curve were determined. The duration of tendon loading was calculated as the time during which the tendon force was > 100 N (which represents ~3% of maximal tendon force at the walk and 2% at the trot); this threshold was also used for the calculation of the area under the tendon force-time curve.
Statistical analysis To compare the effects of the two surfaces on the parameters studied and to adjust for repeated measurements within each horse, linear mixed-effects regression models were used (SAS version 9.2). Results were considered to be significant when P values were < 0.05.
Results The five horses were significantly slower on sand than asphalt, both at the walk (speed mean ± SD: sand 1.58 ± 0.14 m/s; asphalt 1.61 ± 0.12 m/s; P = 0.0478) and at the trot (sand 3.12 ± 0.36 m/s; asphalt 3.41 ± 0.46 m/s; P < 0.0001). As a consequence, stride duration was longer on sand than asphalt (P = 0.0008 at the walk; P < 0.0001 at the trot; Table 1). The average tendon force-time curves of each horse on both surfaces are presented in Figs. 2A and
2B. At the walk, the tendon force-time curve typically showed two peaks, the first one always being the highest, whereas a single peak was present at the trot. Although this general shape was observed in all horses, inter-individual variations in the SDFT loading pattern were apparent at both gaits.
Although there was a lower speed on sand, the maximal tendon force was higher on this surface than on asphalt at the trot (+6%; P = 0.037); at the walk, there was no significant difference between sand and asphalt at the first or second peaks (Table 1). The time of maximal tendon force was delayed on sand at both gaits (and for both peaks at the walk), when expressed in seconds (+9% in average; P < 0.0001 in all cases); when time was expressed in % of stride duration, the difference between surfaces was significant only at the walk (P < 0.0001 for both peaks). The duration of tendon loading was longer on sand (mean +5% when expressed in seconds and +2% when expressed as % of stride duration; P < 0.001 in all cases except at the trot when expressed in % of stride duration, where P = 0.060). The area under the tendon force-time curve was larger on sand (+10% in average), both at the walk (P = 0.043) and trot (P < 0.0001).
Figs. 3A and 3B show the average vertical component of the GRF (GRFz) measured with the DHS vs. time, for the two horses in group 2. Both GRFz peaks were lower on sand than asphalt at the walk (mean ± SD: first peak on asphalt 3434.8 ± 294.4 N vs. sand 3312.1 ± 204.7 N, P = 0.013; second peak on asphalt 3715.1 ± 357.7 N vs. sand 3652.3 ± 345.0 N, P = 0.016) and the single peak at the trot (asphalt 5901.4 ± 226.1 N vs. sand 5771.0 ± 230.8 N, P = 0.001).
Discussion
Significant differences in loading of the equine SDFT on a soft ground surface compared with an asphalt surface were demonstrated in this study using the non-invasive ultrasonic technique. SDFT force values were obtained after calibration of the SOS values directly measured with the device. In both groups of horses, the calibration procedure was based on the linear relationship previously demonstrated in vitro between the force applied to forelimbs vertically compressed in a standing position and the corresponding SDFT force (Jerbi et al., 2000). This relationship was determined by combining limb compression tests (on four left forelimbs isolated at the distal third of the humerus) with SDFT traction tests (isolated from the same limbs). The four horses used in the study of Jerbi et al. (2000) had characteristics (mean body mass 557 ± 83 kg; mean age 8.8 ± 1.7 years) similar to those of the five horses in the present study, although the breed of horse was different; Jerbi et al. (2000) used French Warmbloods, whereas the present study used French trotters.
Using a unique ratio (0.76) to convert limb compression force (or GRFz) to SDFT force may lead to systematic errors in the tendon force calculation in a given horse, since this ratio is likely to be dependent on the conformation of each horse and on the structural and material properties of the SDFT. Furthermore, this ratio was determined in vitro, neglecting the participation of the SDF muscle and assuming that distal limb kinematics during compression tests are the same as in vivo during mid-stance, which is likely to be an oversimplification. However, it should be noted that Takahashi et al. (2010), combining the use of an arthroscopically implantable force probe in the SDFT and force plate measurements in seven thoroughbreds at the trot (3 m/s), found a ratio of maximum SDFT force to maximum GRFz of 0.82 ± 0.24, which is similar to the value used here.
Taking into account the variability of the ratio (0.76 ± 2 SD), it can be demonstrated that the difference (in N) in the SDFT force between sand and asphalt varies by ± 34%. In other words, a difference of 100 N between sand and asphalt with a 0.76 ratio would become 66 N with a 0.5 ratio and 134 N with a 1.02 ratio. However, the ratio value has no impact on the relative difference between surfaces (i.e. when the force difference is divided by the SDFT force on asphalt) and thus no effect on the average increase of 6-7 % in the SDFT peak force observed here on sand compared with asphalt. Furthermore, the ratio has no impact on the SDFT loading pattern. Thus, the inter-individual variations in the SDFT loading pattern apparent in the present study, both at the walk and trot, which confirm previous observations made from invasive measurements (Jansen et al., 1993), would not be affected if a subjectspecific ratio had been used.
Calibration of SOS measurements using the GRFz pattern previously established on another equine population, instead of the simultaneously measured vertical force from the same horse, also introduces an error, as discussed by Vergari et al. (2012b). In the present study, using the previously established GRF pattern in group 2 horses would lead to an overestimation of the SDFT peak force difference between the two surfaces by 8% on average at the walk and trot (i.e. a difference of 6% between sand and asphalt, when measured using the DHS, would become 6.5%).
Although the values of SDFT force obtained in the present study are affected by the approximations and errors mentioned above, these values are consistent with those obtained in horses using invasive devices, both at the walk and trot (Lochner et al., 1980; Butcher et al., 2007; Takahashi et al., 2010). Furthermore, since the same relation was applied to all trials of a given horse, under the assumption that the SDFT SOS-force relationship is
reproducible in a given tendon (Crevier-Denoix et al., 2009b), the calibration procedures used here should not affect the comparison between surfaces.
The present study demonstrated an overall increase in SDFT loading on sand compared with asphalt; the duration of tendon loading and the area under the tendon forcetime curve were significantly increased on sand, both at the walk and trot, and tendon maximal force was significantly higher on sand at the trot. This SDFT loading increase was observed even though the horses were generally slower on sand and (in the two DHS equipped horses) while the simultaneously measured GRFz was decreased on sand.
The increased stride duration measured on sand has also been described by Riemersma et al. (1996b) in ponies (weighing 165-240 kg) on a loose sand track compared with pavement. Although no significant effect of ground surface type on the selected SDFT loading parameters could be demonstrated by Riemersma et al. (1996b), the tendon strain charts presented by these authors are similar to those of our study; the SDFT loading (expressed as SDFT strain) duration was increased on sand both at the walk and trot, as was the second peak of SDFT strain at the walk and, to a lesser extent, the single peak at the trot. Times of maximal strain (in % of stride duration) were also delayed, as in the present study. The absence of a significant difference between types of ground surface at the walk can be explained by the fact that Riemersma et al. (1996b) only considered the maximal SDFT strain, i.e. only the first peak of the curve, for which no significant difference was observed in the present study, contrary to the second peak.
The absence of a significant difference in strain on the SDFT between types of ground surface obtained by Riemersma et al. (1996b), although somewhat in contradiction with the
presented charts, could be explained by the distal limb conformation of ponies. Ponies have small feet, with relatively high heels and a short toe, which implies a reduced lever arm of the GRF acting on the distal interphalangeal joint. Furthermore, ponies have a less ample propulsion phase of the stance compared with horses, which minimises the digital joint angle changes observed during this phase. Maximal SDFT forces measured by Riemersma et al. (1996b) in ponies at the walk (~2.2-2.6 N) and slow trot (~6.7 N/kg) were lower than those obtained in horses (~6-7 N/kg at the walk; 8.5-11 N/kg at the trot) in the present study and by other authors (Lochner et al., 1980; Butcher et al., 2007; Takahashi et al., 2010; Vergari et al., 2012b). This may also have a link with the more subtle effects on the SDFT recorded in ponies (vs. horses) when changing ground surface or hoof angle (Riemersma et al., 1996a and b).
Riemersma et al. (1996b) measured the angle between the sole of the hoof and the ground surface at the walk on sand and demonstrated a small positive caudal angle, i.e. a hoof orientation similar to an elevation of the heels. In all ponies, this heel elevation hoof orientation increased during the stance phase by 4.8-12.6 °. Compared with the situation on asphalt, where the hoof cannot penetrate the ground surface, this forward rotation on sand implies an increased distal interphalangeal flexion, which has been confirmed by kinematic studies (Scheffer and Back, 2001). Since distal interphalangeal joint flexion provokes DDFT release, this movement is accompanied by dropping of the fetlock (extension), as demonstrated in standing horses (Denoix, 1985; Crevier-Denoix et al., 2001) and horses at the walk (Chateau et al., 2004); this in turn increases SDFT and SL loading (Denoix, 1994). Active contraction of the flexor muscles at the end of stance (propulsion phase), which is necessarily increased on a soft, less reactive, ground than on a firm surface, is also expected to increase the SDFT loading further.
It is now established that firmer surfaces are a risk factor for SDFT injuries in race horses (Williams et al., 2001; Reardon et al., 2012), probably because of an increased SDFT loading rate at high speed. The results of the present study nevertheless demonstrate the rationale of rehabilitating SDFT injuries on firm ground surfaces at slow gaits.
Conclusions The results of this study demonstrate that the SDFT loading is significantly affected by ground surface, with increased loading on sand compared with asphalt. The combined increases in maximal SDFT force, duration of tendon loading and area under the tendon force-time curve during stance observed in the present study are consistent with the clinical observations that horses suffering from SDFT injuries generally do not show improvement of their lameness when examined on soft ground.
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 The authors thank the Conseil Régional de Basse-Normandie, the Fonds Unique Interministériel, the French Ministry of Agriculture, the Fonds Européen de Développement Régional (FEDER) and the Institut Français du Cheval et de l’Equitation (IFCE) for their financial support for this project. We are very grateful to Fabrice Cavé and Jean-Michel Goubault, farriers (IFCE), as well as Elodie Paumier-André, technician (CIRALE), for their participation, and to the CIRALE and IFCE for loaning horses. The authors also thank
Romuald Glowacki and the Pôle de Compétitivité Hippolia for their logistical and administrative support, as well as Guy Launay for assistance with the manuscript.
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Table 1 Mean and standard deviation (SD) of stride duration and superficial digital flexor tendon loading variables measured in five horses at the walk and trot alternately on asphalt and on a sand and fibre mix (sand) surface.
Stride duration (s) Maximal tendon force (walk first peak) (N) Maximal tendon force (walk second peak) (N) Time of maximal tendon force (walk first peak) (s) Time of maximal tendon force (walk second peak) (s) Time of maximal tendon force (walk first peak) (% of stride duration) Time of maximal tendon force (walk second peak) (% of stride duration) Duration of tendon loading (s) Duration of tendon loading (% of stride duration) Area under the tendon-force time curve (Ns)
* Significant differences between surfaces: P < 0.05.
Asphalt (n = 117) Mean SD 1.156 0.053 3517.6 480.1 2076.0 629.8 0.158 0.018 0.422 0.046 13.9 1.6 36.7 3.7 0.613 0.072 52.9 4.4 1172.7 201.7
Walk Sand (n = 121) Mean SD 1.178 0.057 3609.7 548.8 2216.8 573.3 0.179 0.026 0.455 0.042 15.6 2.2 38.9 4.0 0.641 0.073 54.4 4.5 1278.6 223.4
Trot
P* < 0.01 0.5 0.1 < 0.01 < 0.01 < 0.01 < 0.01 < 0.01 < 0.01 < 0.05
Asphalt (n = 182) Mean SD 0.717 0.043 4715.6 572.0
Sand (n = 156) Mean SD 0.749 0.043 4976.3 339.8
P* < 0.01 < 0.05
0.150
0.019
0.159
0.023
< 0.01
21.0
2.3
21.3
2.9
0.2
0.259 36.0 820.7
0.031 2.8 133.8
0.274 36.4 907.5
0.036 3.2 133.8
< 0.01 0.06 < 0.01
Figure legends
Fig. 1. Experimental device to study the effects of ground surface on the superficial digital flexor tendon loading in horses at the walk and trot. The right forelimb of each horse is equipped with an ultrasonic probe (1 MHz) facing the palmar metacarpal area. The probe, covered with acoustic gel, is inserted in an adapted (windowed) tendon boot and placed in contact with the skin (A). The probe in the boot is maintained by an elastic band and connected to an electronic module placed on the saddle. In two horses, the right forehoof was also equipped with a dynamometric horseshoe composed of four triaxial piezoelectric force sensors (B); the vertical component of the ground reaction force (GRFz) was directed proximo-distally (perpendicular to the plane of the shoe). The corresponding electronic devices are placed in saddle-bags. A WiFi-connection is used to acquire data remotely.
Fig. 2. Force in the superficial digital flexor tendon of the right forelimbs of five horses at the walk (A) and trot (B) on asphalt (dark grey) and on a sand and fibre mix (sand) surface (light grey) during averaged strides (n = 19-34 strides per horse on each surface at the walk; n = 2157 strides per horse at the trot). The time bases are standardised to a complete stride.
Fig. 3. Vertical component of the ground reaction force (GRFz) measured with a dynamometric horseshoe placed on the right forehoof of two horses at the walk (A) and at the trot (B) on asphalt (dark grey) and on a sand and fibre mix (sand) surface (light grey) during averaged strides (n = 24-34 strides per horse on each surface at the walk; n = 44-57 strides per horse at the trot). The time bases are standardised to a complete stride.
