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Effect of Fatigue on Equine Metacarpophalangeal Joint Kinematics—A Single Horse Pilot Study
Journal Pre-proof Effect of fatigue on equine metacarpophalangeal joint kinematics – a single horse pilot study Brenna R. Pugliese, Cristina T. Carballo, Kevin M. Connolly, Melissa R. Mazan, Carl A. Kirker-Head PII:
S0737-0806(19)30598-2
DOI:
https://doi.org/10.1016/j.jevs.2019.102849
Reference:
YJEVS 102849
To appear in:
Journal of Equine Veterinary Science
Received Date: 12 March 2019 Revised Date:
30 July 2019
Accepted Date: 7 November 2019
Please cite this article as: Pugliese BR, Carballo CT, Connolly KM, Mazan MR, Kirker-Head CA, Effect of fatigue on equine metacarpophalangeal joint kinematics – a single horse pilot study, Journal of Equine Veterinary Science (2019), doi: https://doi.org/10.1016/j.jevs.2019.102849. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Inc.
Original Research Effect of fatigue on equine metacarpophalangeal joint kinematics – a single horse pilot study
Brenna R. Pugliese, Cristina T. Carballo, Kevin M. Connolly, Melissa R. Mazan, Carl A. Kirker-Head
Orthopaedic Research Laboratory, Cummings School of Veterinary Medicine at Tufts University
Corresponding author: Carl Kirker-Head, MA, Vet MB, MRCVS, DACVS, DECVS Department of Clinical Sciences 200 Westborough Road North Grafton, MA 01536, USA Email: [email protected] Telephone: 508-839-7926 Fax: 508-839-7922
Author emails: B.R. Pugliese, [email protected]; C.C. Carballo, [email protected]; K.M. Connolly, [email protected]; M.R. Mazan, [email protected]
CONFLICT OF INTEREST STATEMENT Dr. Carl Kirker-Head has received financial remuneration as a consultant from the study sponsor HorsePower Technologies, Inc. (Lowell, MA, USA).
Highlights •
The treadmill exercise regimen consistently induced metabolic fatigue
•
Electrogoniometry successfully generated metacarpophalangeal joint kinematic data
•
Metacarpophalangeal joint extension angle increased with fatigue
•
Stride duration increased with fatigue
CRediT Author Statement Brenna R. Pugliese: Methodology, Validation, Formal Analysis, Investigation, Data Curation, Writing – Original Draft, Writing – Review & Editing, Visualization, Project Administration. Cristina T. Carballo: Conceptualization, Methodology, Validation, Investigation, Data Curation, Writing – Original Draft, Writing – Review & Editing, Project Administration. Kevin M. Connolly: Formal Analysis, Investigation, Data Curation, Writing – Review & Editing, Visualization. Melissa R. Mazan: Conceptualization, Methodology, Investigation, Writing – Review & Editing, Supervision. Carl A. Kirker-Head: Conceptualization, Methodology, Investigation, Writing – Original Draft, Writing – Review & Editing, Visualization, Supervision, Project Administration, Funding Acquisition.
Abstract The objective was to validate a scientific method for characterizing equine metacarpophalangeal joint (MCPJ) motion in the non-fatigued and fatigued states using a single horse at trot, slow canter, and fast canter. One healthy Thoroughbred gelding exercised on a treadmill to exhaustion [fatigued state] (heart rate >190 BPM and blood lactate >10 mmol/L) while bilateral MCPJ angular data were acquired using electrogoniometry. Blood lactate and heart rate reflected transition from non-fatigued to fatigued states with increasing exercise duration and treadmill speed. Electrogoniometry consistently demonstrated: increase in mean MCPJ maximum extension angle with onset of fatigue; altered extension and flexion angular velocities with onset of fatigue; and increasing stride duration and decreasing stride frequency with onset of fatigue. The method allowed a preliminary but comprehensive characterization of the dynamic relationship between MCPJ kinematics and fatigue, prompting the need for multisubject studies that may enhance our ability to moderate exercise-related distal limb injury in equine athletes.
Keywords: equine; metacarpophalangeal joint; kinematic; fatigue; electrogoniometry
1. Introduction
The horse is an accomplished athlete largely by virtue of a conformation evolved to enhance locomotor efficiency. Yet these musculoskeletal adaptations predispose to injury, particularly in the proximity of the metacarpophalangeal joint (MCPJ) where there is a higher incidence of traumatic and degenerative lesions than elsewhere in the body [1-3]. The propensity for injury is exacerbated by metabolic fatigue [4], a complex physiological response to exercise resulting in an inability to sustain constant activity level [5]. Clinical observation implies that fatigue can induce substantial MCPJ hyperextension, yet only one scientific study [6] performed in Standardbreds briefly reports that fatigue increased MCPJ maximum extension angle by 5° during the trot on a treadmill. That limited characterization of MCPJ kinematics in the fatigued horse substantially limits our understanding of how trauma may be a sequela of fatigue-related alterations in locomotor pattern: muscle fatigue decreases muscular force development and contraction velocity and adversely alters neural feedback [7] leading to potentially injurious kinematic gait changes. A more precise characterization of the relationship between MCPJ motion and fatigue across a range of gaits may eventually enhance our ability to moderate exercise-related injury. This pilot study had several objectives: to validate a scientific method, specifically a treadmill exercise regimen as a means of inducing metabolic fatigue and electrogoniometry as a means of measuring equine MCPJ motion; further, we sought to comprehensively characterize sagittal plane MCPJ motion and temporal values at the trot, slow canter, and fast canter in this single horse in the non-fatigued and fatigued states, all as a prelude to conducting similar studies using a greater number of subjects.
2. Materials and Methods
2.1 In vitro data acquisition and technique validation 2.1.1
Animal. A single fresh equine cadaver distal forelimb, transected at mid-radius, was
harvested from an adult horse (~450 kg) euthanized at the Cummings School of Veterinary Medicine for reasons other than orthopedic pathology. To prepare the limb for testing, transection of the suspensory ligament, deep digital flexor tendon, and superficial digital flexor tendon was completed at mid-metacarpal III (MCIII) level to increase the available range of MCPJ motion (ROM) (81 degrees). The limb was positioned in lateral recumbency with the segment proximal to the MCPJ firmly immobilized. The segment of the limb distal to the MCPJ was allowed unrestricted movement in the sagittal plane (extension and flexion). 2.1.2
Instrumentation. A single 150-mm type electrogoniometeri and general-purpose
amplifierii were used to collect angular data onto a laptop computer. In every case, the electrogoniometer endblocks were secured to the limb using circumferentially applied elastic tapeiii like that subsequently used in vivo (see section 2.2.2 to follow). Three fixation methods were evaluated: i. Free coil - The hard plastic endblocks were secured to the limb but the flexible coil remained free; ii. Stockinette coil - As for ‘i’ above but the entire unit was additionally placed under a snug stockinette sock; and iii. Tunneled coil - As for ‘i’ above but the coil was additionally placed in a thin, soft fabric tunnel. 2.1.3
Imaging and signal calibration method. A fluoroscopy unitiv was placed perpendicular
to the cadaver limb and centered over the MCPJ to capture latero-medial images of the MCPJ at angles spanning from maximum extension to maximum flexion. The angles derived from the fluoroscopic images were subsequently used in a two-point calibration system to transform the simultaneously-derived electrical data collected from the electrogoniometers into degree units.
Medical imaging softwarev was used to measure the MCPJ angle from the fluoroscopic images. Using the Measurement software tool, a circle was overlaid on the condyle of distal MCIII, and the center of this circle was determined to be the MCPJ center of rotation (COR, MCPJ-COR). Lines were drawn from the mid-shaft of MCIII to the MCPJ-COR and again from the MCPJCOR to the mid-shaft of the distal first phalanx (P1). The angle between the two lines, as measured using the Markup Angle software tool, was subtracted from 180 to obtain the MCPJ angle. 2.1.4
Validation experiment. For each fixation method, the electrogoniometers were calibrated
6 times and on each occasion, 3 electrogoniometer-derived angles were determined (18 angles in total per treatment, except in treatment ii, where there were only 17 data points). The 3 angles recorded for the MCPJ for each fixation method corresponded to the maximum extension angle, the maximum flexion angle and a neutral angle between both extremes. For each of the 3 angular positions, MCPJ angle was derived concurrently from the electrogoniometer and from the fluoroscopic image. 2.1.5
Statistical analysis. The mean and standard deviation of the difference in angles
recorded by each modality (electrogoniometer and fluoroscopy) upon each calibration (n=6 per treatment group) was reported in this study to reflect the accuracy and repeatability of the electrogoniometer system as it reports MCPJ angle. To further characterize the method agreement, Paired t-tests were used to compare the angles obtained from the fluoroscopy unit with those obtained from the electrogoniometer for each fixation method. For the treatments where there was no statistical difference (p>0.05), indicating that there was no evidence of a systematic difference or bias, the coefficient of reliability was calculated to investigate the agreement between the fluoroscopy and electrogoniometry derived angles.
2.2 In vivo data acquisition 2.2.1
Animal. One healthy ‘off-the-track’ Thoroughbred gelding (6 years, 540±30 kg, 164 cm
at the withers) was used in all procedures approved by Tufts University’s Institutional Animal Care and Use Committee. The animal entered the program ‘racing fit’ two months prior to testing, during which time it acclimated to high-speed treadmillvi exercise five times weekly to maintain fitness. 2.2.2
Instrumentation. 150 mm single axis electrogoniometersi transformed the angular
position of the MCPJ in the sagittal plane (extension and flexion) into a proportional electrical signal with a sampling rate of 2000 Hz. The electrogoniometers were bilaterally affixed to the dorsal aspect of the MCPJ using circumferentially applied elastic tapeiii to secure the endblocks to mid-MCIII and to distal P1, respectively (free coil fixation method as in (i) above). The flexible coil spanned only the MCPJ. The proximal endblock was attached to a 3-meter-long extension cable directly connected to a general-purpose amplifierii, which allowed for augmentation of the electrical signal recorded by the laptop computer. The extension cable was affixed to the distal antebrachium using circumferentially applied elastic tape, and it was dorsally secured to the saddle using hook and loop fastenersvii. 2.2.3
Intra-session signal calibration method. Two latero-medial radiographs were taken of
each MCPJ following electrogoniometer placement, one with the joint in extension and one with the joint in flexion (Fig. 1a and 1b). The technique described to measure MCPJ angle from fluoroscopic images (see section 2.1.3) was similarly employed to measure MCPJ angle from the radiographs of the standing horse’s limb in both positions. The MCPJ angles derived from the standing and flexed images were used in a two-point calibration to transform the data into
degree units, by in-putting these values in the electrogoniometer software’s calibration functionviii. Calibration was performed prior to commencement of each of the 5 events. 2.2.4
Definition of MCPJ Angle. MCPJ angle, as measured by electrogoniometry, corresponds
to the angle between the long axes of MCIII and P1 (Fig. 2). The zero-degree point is the single line of best fit drawn parallel to the long axis of MCIII and P1 and passing through the MCPJ center of rotation (COR) and is used as a reference; a positive angle describes extension while a negative angle describes flexion. Maximum extension angles (most positive) were derived from stance phase angular data. Maximum flexion angles were the minimum (most negative) angles registered during the swing phase. 2.2.5
Exercise regimen. Data were collected for 5 standardized events [5 separate testing days,
one test per day, one week apart]. Each test took the horse from the non-fatigued to fatigued state through a series of graduated gaits and speeds. A 28.1 kg saddle and pad were secured on the horse’s back to increase exercise intensity. Warm-up consisted of walking exercise for 5 minutes (6.0 kph) followed by trotting for 5 minutes (10.7 kph) at 0o incline. The treadmill was then inclined to 6o for data collection. There followed a 1 minute fast canter (35.1 kph), 1 minute slow canter (24.1 kph), and 1 minute trot (10.7 kph) sequence, each preceded by 5 minutes of walking (6.0 kph) to normalize parameters. This provided for acquisition of nonfatigued data. The horse was then maintained at a fast canter (35.1 kph) for 8 minutes as exhaustion (fatigue) visibly ensued before immediately returning to a slow canter (1 minute) and trot (1 minute). The latter 3 test speeds were completed in the fatigued state as confirmed by heart rate and blood lactate analysis. 2.2.6
Fatigue status assessment. Metabolic variables were assessed during the last 15 seconds
of each exercise segment. Heart rate (beats per minute/BPM) was measured using cardiac
telemetryix. Blood lactate (millimols per liter/ mmol/L) was simultaneously measuredx using blood drawn from the catheterizedxi right jugular vein. Fatigue was confirmed with a heart rate >190 BPM, a maximum whole blood lactate >10 mmol/L, and the need for the horse to receive verbal encouragement to maintain pace with the treadmill [8]. Reported mean ± standard deviation (SD) heart rate and lactate for each condition were calculated across the five independent testing events, each one week apart. 2.2.7
Data Processing. An MP150 Data Acquisition System and AcqKnowledge softwareviii,
were used to generate real time MCPJ angle (degrees) vs time (seconds/sec) graphs. 2.2.8
Data Analysis. Thirty consecutive strides were analyzed for trot, slow canter and fast
canter for the non-fatigued and the fatigued states in both forelimbs on each of the five testing days. The first thirty strides of the non-fatigued conditions, and the last thirty strides of the fatigued conditions were assessed. Reported mean data were calculated across five independent testing events for the left leg and across three independent testing events for the right leg (a result of electrogoniometric equipment failure on two occasions). The horse always cantered on the left lead with the “lead limb” referring to the horse’s left foreleg and the “non-lead limb” referring to the right foreleg. Reported kinematic and temporal variables include mean ± standard error (SE): MCPJ maximum extension and flexion angle (degrees, deg), maximum extension and flexion angular velocity (degrees per second, degrees/sec), stride duration (milliseconds, msec) and stride frequency (strides per minute, str/min). Increase (percent, %) of MCPJ extension angles in the fatigue state over non-fatigued extension values were calculated as (ⱷfatigued x 100/ⱷnon-fatigued). 2.2.9
MCPJ Angular Velocity. Angular data was duplicated and transformed using
AcqKnowledge Software; the resultant waveform described angular velocity (deg/sec). The
maximum extension angular velocity (positive value) reported in this study corresponded to the maximum MCPJ velocity as it extended in stance phase. The maximum flexion angular velocity reported is the minimum (most negative) MCPJ velocity as it flexed in swing phase. 2.2.10 Stride Duration and Stride Frequency. Stride duration (ms) was calculated as time from one maximum extension angle to the next. Stride frequency was calculated as strides per minute (str/min). 2.2.11 Statistical analysis. To model these outcomes and adjust for the correlation among strides for each test, a mixed effects model was used for each outcome with limb/side, gait, fatigue state, and test as the predictors. A compound symmetry variance-covariance matrix was assumed and generated the least-squares (LS) means for each outcome to test the difference between the fatigued vs. non-fatigued state within limb/side and gait. Because LS means are derived statistics that tend to be normally distributed, a t-test was used to compare the LS means as above, as well as a Tukey adjustment for multiple comparisons. The standard calculation was used for the coefficient of variation within each limb, gait, fatigue state, and test to demonstrate the consistency of the measurements and of the variability. Metabolic data (heart rate and whole blood lactate) were compared in this single horse using descriptive statistics.
3. Results
3.1 In vitro data acquisition and technique validation Differences between pairs of MCPJ angles derived from i) fluoroscopic still images (regarded as the gold standard in this comparison) and ii) electrogoniometry were calculated and found to be normally distributed. The mean difference (in degrees) for each calibration (6 per treatment) was 2.14˚ for the free coil, 2.38˚ for the stockinette coil, and 2.87˚ for tunneled coil treatments (Table 1). There was a significant difference (P = 0.01) between the fluoroscopy-
derived angles and those derived using the electrogoniometer when the latter was applied to the limb using the tunneled coil technique. No significance was found between fluoroscopy-derived and electrogoniometry-derived measurements when using the free coil treatment (P = 0.25) or the stockinette coil treatment (P = 0.16). (Table 1). Since a significant difference between the angle calculation modalities in the free coil and stockinette coil treatments was not detected, the reproducibility coefficient (2 times the standard deviation of the differences) for these treatment groups was calculated to summarize the lack of agreement. The reproducibility coefficient for the mean difference within each set of angles and upon each calibration of the goniometers (n=6) was 1.83 for the free coil and 2.11 for the stockinette coil treatment (Table 1). The free coil was therefore selected as the most accurate and repeatable electrogoniometric technique and was subjected to further testing in vivo.
3.2 3.2.1
Metabolic Analysis The treadmill exercise regimen was well-accepted by the horse and consistently
prompted blood lactate values that reflected a transition from a non-fatigued state on completion of the initial one minute fast canter, slow canter and trot sequences, to a fatigued state [9, 10], starting as the horse progressed through the 8 minute fast canter and persisting through the end of the treadmill activity (fatigued trot) (Fig. 3). Mean ± SD blood lactate increased from 5.30 ± 1.24 mmol/L at the non-fatigued fast canter to 10.06 ± 3.10 mmol/L at the fatigued fast canter, continuing to rise during the subsequent transition from fatigued fast to slow canter (16.84 ± 2.44), reflecting a lag between fast canter exercise and the accompanying peak in lactate.
Lactate thereafter decreased during the fatigued trot (14.58 ± 1.85) though it remained well above baseline (1.38 ± 0.50) non-fatigued trot values. Mean ± SD heart rate (BPM) increased and decreased with increases and decreases in speed (Fig. 3). Heart rate was consistently elevated in the fatigued versus the non-fatigued states for the fast canter (201.6 ± 14.5 vs 170.8 ± 26.8), slow canter (180.33 ± 25.74 vs 158.80 ± 5.02), and trot (139.67 ± 8.14 vs 133.40 ± 20.77).
3.2.2
Kinematic Analysis The electrogoniometers required diligent preparation and placement to successfully
generate consistent data. Displacement of the goniometer under its adhesive tape eliminated right forelimb data in two of five trials. The kinematic data is reported in two formats: 1) Mean ± SE by gait, limb and fatigue status; and 2) quantitative difference between non-fatigued and fatigued data by gait and by limb (Tables 2 and 3). Lead (left) limb mean ± SE maximum extension angle (deg) consistently increased significantly (P < 0.0001) with fatigue at trot (60.15 ± 2.98 vs 64.60 ± 5.09), slow canter (71.49 ± 5.42 vs 82.83 ± 6.97), and fast canter (85.30 ± 6.49 vs 92.69 ± 8.46). Non-lead (right) limb mean ± SE maximum extension angle (deg) also increased significantly (P < 0.0001) with fatigue at trot (67.03 ± 2.29 vs 74.37 ± 2.97), slow canter (75.97 ± 1.77 vs 87.04 ± 3.59), and fast canter (75.98 ± 2.02 vs 88.72 ± 3.00). Fatigue did not produce consistent change (P>0.05) in mean ± SE maximum MCPJ flexion angles (deg) for trot (-26.92 ± 3.07 vs -25.28 ± 5.60) and fast canter (-35.35 ± 1.24 vs 35.89 ± 4.57) in the lead (left) limb, nor for trot (-22.46 ± 2.46 vs -21.07 ± 3.54) and slow canter
(-17.87 ± 1.66 vs -16.87 ± 3.14) in the non-lead (right) limb. However, in the lead limb fatigue prompted a significant (P=0.01) increase in maximum flexion angle at the slow canter (-26.35 ± 2.78 vs -28.18 ± 5.86). In the non-lead limb, fatigue significantly (P<0.0001) decreased MCPJ flexion angle at fast canter (-32.53 ± 1.29 vs -25.12 ± 2.43). With regard to angular velocity data, derived only from the lead limb, moderate changes were also noted with fatigue. For trot, fatigue prompted a significant (P < 0.0001) increase in mean ± SE maximum extension angular velocity (deg/sec) (1053.85 ± 37.37 vs 1577.29 ± 109.96) and corresponding significant (P < 0.0001) decrease in mean maximum flexion angular velocity (-1464.47 ± 51.54 vs -1343.16 ± 55.14). The pattern was repeated for slow canter, with mean maximum extension angular velocity significantly (P=0.008) increasing (1971.87 ± 60.39 vs 2032.53 ± 118.31) and mean maximum flexion angular velocity significantly (P < 0.0001) decreasing (-1940.80 ± 42.30 vs -1719.49 ± 52.34) with fatigue. At the fast canter, significant differences in angular velocity persisted but fatigue prompted a reversal in the direction of change with mean maximum extension velocity significantly (P < 0.0001) decreasing from 4879.54 ± 700.56 in the non-fatigued state to 4565.95 ± 547.07 in the fatigued state. Mean maximum flexion angular velocity did not significantly change with onset of fatigue at the fast canter (P=0.19).
3.2.3
Temporal Analysis Fatigue significantly (P<0.0001) increased mean ± SE stride duration (ms) at trot
(716.73 ± 3.23 vs 735.15 ± 0.91), slow canter (563.98 ± 1.33 vs 603.75 ± 1.21), and fast canter (504.55 ± 1.95 vs 541.96 ± 1.91). Fatigue significantly (P<0.0001) decreased mean ± SE stride
frequency at the trot (83.72 ± 0.38 vs 81.62 ± 0.10), slow canter (106.39 ± 0.25 vs 99.38 ± 0.20), and fast canter (118.92 ± 0.46 vs 110.71 ± 0.39).
4. Discussion
The treadmill exercise regimen was well tolerated by the horse and the regimen generated consistent data that confirmed the onset of fatigue, allowing correlation of metabolic state to MCPJ kinematics and temporal values. Increased blood lactate and heart rate parameters were consistent with values from previous reports of horses transitioning from a non-fatigued to fatigued state. The increase in lactate concentration with speed reported in this study has been previously documented [9-11] and, in this regard, the maximum mean whole blood lactate concentration reported during the fatigued canter (16.84 mmol/L) is consistent with previously published plasma lactate data (20.5 mmol/L) [10], recognizing that whole blood lactate corresponds to approximately 70% of plasma lactate values (0.7*20.5 mmol/L = 14.35 mmol/L). The increase in heart rate with speed of locomotion reported herein has also been previously described [9, 11], and the mean peak heart rate of 201.6 BPM during the fatigued fast canter is comparable to 212 BPM reported by Schuback et al. [10]. Subjectively, the onset of fatigue in this study was also characterized by the horse requiring verbal encouragement to keep pace with the treadmill [8], similar to human exercise studies in which volitional fatigue is the usual endpoint of an exercise test with considerable verbal encouragement being given to the subject [12]. Electrogoniometry is uncommonly applied in the horse and only 3 different authors report its use in characterizing MCPJ motion [13-19]. However, flexible electrogoniometry is widely accepted as a means of reliably collecting kinematic and temporal data across a range of functional activities in humans [20, 21]. Electrogoniometry has been validated in both the
human ankle [22] and wrist [23] as an accurate and cost-effective method for the clinical researcher as recently as 2018. Similar studies in canines have identified electrogoniometry as a suitable and sensitive instrument for measurement of joint angle in the distal limb [24, 25]. Though more complex modalities such as high-speed videography and marker-based motion analysis systems are widely available, we inferred from studies in human patients [22] that flexible electrogoniometry could provide the equine researcher with a more practical and financially affordable method to collect and interpret data. Hence, a cadaver limb validation of the BIOPAC electrogoniometer system was performed to determine the optimal method of MCPJ application as well as the accuracy of this method in the equine subject. This in vitro phase preceded live horse testing and evaluated the agreement between data obtained from each of 3 methods of electrogoniometer application (free coil, stockinette coil, tunneled coil) and a fluoroscopic method of angle analysis. The mean of the differences for each treatment represents a measure of accuracy, or how closely the angles derived from the electrogoniometers are to the real angles (as measured by the fluoroscopy unit), and the reproducibility coefficient is a measure of repeatability of the treatments. The free coil method of electrogoniometer attachment to the skin was the most accurate: average deviation from the true angle was 2.14°. This finding is similar to the accuracy of ±2˚ reported by the manufacturer. It was also the most repeatable as 95% of the differences fell within 1.83° of the mean difference (reproducibility coefficient). The free coil technique outperformed the stockinette coil method in both accuracy (2.14 vs 2.38) and repeatability (1.83 vs 2.11) and was therefore selected for in vivo testing. The tunnel coil method was the only treatment with a significant difference (p<0.05) between the electrogoniometer- and fluoroscopy-derived angles.
Consequently, the stockinette and tunnel methods described herein should not be used for equine MCPJ motion analyses in future studies. In the current study, the in vivo system employing the free coil method generated repeatable data but set-up required diligence and attention to detail. Even so, displacement of the goniometer under its elastic tape excluded right forelimb data in two of five trials. In subsequent studies, affixation of the end-blocks to the limb using additional means such as cyanoacrylate adhesive of the block to the hair coat could be considered. With skin-secured kinematic systems, it is always important to consider the potential effect of relative skin movement on the measurement of joint angle. Skin displacement might otherwise result in data variability and joint movement has been reported to be overestimated due to the associated soft tissue artifact [26-28]. To correct for this discrepancy, several models have been applied [28-30] while other researchers have resorted to using bone-fixed marker techniques [31, 32]. Fortunately, skin displacement below the carpus is negligible, and does not significantly affect kinematic analysis of the distal limb [28]; therefore, skin movement was not controlled for in this study. When we compared our electrogoniometric data in the non-fatigued horse with that previously generated using skin marker systems, we noted a similar mean MCPJ maximum extension angle (deg) at trot (60.15 versus 57.7, 61, and 50.7) [33-35]. A review of the limited relevant MCPJ electrogoniometric data from previous publications, wherein Ratzlaff reports an extension angle of 51 degrees at the trot in the non-fatigued horse on a level surface [13], also implies the validity of our technique. In the lead limb at slow canter, we report a mean MCPJ maximum extension angle (71.49), within reasonable range of values reported by Back et al., 1997 and Herring et al., 1992 (59.0 and 56.8, respectively). In the non-lead limb, we report
75.97 degrees mean maximum extension, in general agreement with 62.4 degrees reported by Back et al. 1997 [36] given breed, conformational, speed, and treadmill incline differences between studies. Thus, MCPJ electrogoniometry yielded apparently valid kinematic data. The consistency of the values generated by electrogoniometry with accepted standard values derived from skin marker systems gives credence to our measurement technique. In this study, fatigue induced increases in MCPJ maximum extension angle at all gaits. The fatigued trot in this Thoroughbred prompted a mean increase (P<0.0001) in extension angle (4.45° left [lead] limb, 7.34° right [non-lead] limb) compared with the non-fatigued trot, in general agreement with the 5° increase briefly reported in Standardbred trotters [6]. We also report a fatigue-induced increase (P<0.0001) in maximum MCPJ extension angle for slow canter (+10.76° lead limb, +11.98° non-lead limb) and fast canter (+7.40° lead limb, +12.74° non-lead limb), representing a 7-15% increase over non-fatigued extension values as defined using our MCPJ angle measuring protocol (ⱷfatigued x 100/ⱷnon-fatigued). (Table 2) The pathophysiology of tendinopathy in the fatigued equine is likely similar to humans with alterations in proprioception, loss of muscle control, and increase in misstep predisposing to clinical injury. Human acute Achilles tendinopathy, for example, can be caused by overexertion and muscle fatigue [37] which reduces energy absorption by the musculotendinous unit. Resultantly, muscle no longer protects tendon from strain injury [38] and the forces on passive tissues increase [7]. Our increase in mean MCPJ maximum extension angle with fatigue implies an increased strain in one or more elements of the flexor apparatus and associated risk of overload-related tendinopathy and/or desmopathy. Our swing phase data demonstrated no consistent trend in the mean maximum flexion angle between non-fatigued and fatigued states. Review of the human literature reveals similar
variability in limb joint flexion angles in non-fatigued and fatigued human athletes [39-41]. Compromised proprioception and associated loss of limb control secondary to high intensity exercise may contribute to variability in joint flexion data and precipitate injury in both species [42]. In the horse studied here, fatigue consistently induced changes in MCPJ angular velocities. Similarly, in humans, fatigue-induced changes in maximum angular velocity of the ankle joint have been documented and fatigue of the muscles surrounding the ankle effects dynamic stability [43]. Fatigued muscle, which normally acts eccentrically during the stance phase, becomes impaired in its concentric contraction and ability to achieve appropriate joint angle at touchdown [44]. Hence, fatigue-induced changes in equine MCPJ angular velocity may similarly predispose to injury of the joint and regional soft tissue structures. Our horse traveling at constant treadmill speed increased stride duration and proportionally decreased stride frequency in response to fatigue, consistent with previous reports in the equine and human [6, 45-47]. Reduction in stride frequency with fatigue, demonstrated across species, indicates a shift from optimal stride rate to a more metabolically costly state [47]. Speed is the product of stride length and stride frequency [48], and so horses must increase their stride length to maintain pace with the treadmill. This requires a larger vertical impulse and, because peak force is directly related to MCPJ angle [49], a corresponding increase in MCPJ extension, as we documented. Moreover, Walker et al. 2013 suggest that the greater horizontal displacement (i.e. greater stride length) of the horse at extended gaits also produces greater retraction and protraction when compared to collection [50]. This requirement for altered limb trajectory possibly increases stance phase loading forces, and ultimately the propensity for injury. Any or all of the aforementioned mechanisms might contribute to fatigue-
related tendinopathy/desmopathy in the horse, with exercise-induced hyperthermia and intermittent ischemia exacerbating tendon matrix degeneration [51] and injury risk. It is clinically important to recognize that horses fatigued during treadmill exercise respond differently, biomechanically, to those on land. During endurance rides, horses substantially reduce their speed [46] with fatigue. In our study, as previously discussed, constant treadmill speed with a decrease in stride frequency would have necessitated an increase in stride length – a parameter we did not measure directly. Regardless, the effect of speed and/or stride length are difficult to study in isolation since they act together with other constituents such as loading time, duty factor (predictive of peak forces), and muscle activation. This single-horse study provides for the first time a detailed characterization of the relationship between equine fatigue, MCPJ kinematics, and temporal values, but it has limitations. Testing a single Thoroughbred yields data that may not be representative of populations with breed, gait, conformation, age, or training-related differences [52-56]. Our understanding of the effects of fatigue on MCPJ motion could therefore be enhanced in future studies by simultaneous measurement of stance time and/or duty factor [49], peak vertical ground reaction force, and stride length in a diverse population of horses.
5. Conclusions
We present a detailed analysis of sagittal plane MCPJ motion in a single Thoroughbred racehorse in non-fatigued and fatigued states. The exercise regimen successfully and repeatably induced a transition from non-fatigued to fatigued states, which was effectively confirmed using the metabolic testing methods. The increases in MCPJ extension with fatigue, consistently recorded using electrogoniometry, may have significant clinical implications because hyperextension of the MCPJ likely increases the peak strain on the flexor tendons and
suspensory apparatus, predisposing these structures to overloading, accumulated microdamage, and ultimate tissue rupture [57, 58]. Importantly, hyperextension can also lead to fracture of the proximodorsal aspect of P1, palmar metacarpal condyles, and/or proximal sesamoid bones [5961]. Hence, characterization of MCPJ kinematics and gait temporal values in this preliminary study contributes an initial understanding of the effect of fatigue on joint motion and the implications for distal limb injury. Studies using a larger number of subjects and an expanded series of parameters are now appropriate.
Acknowledgements Kathy Trout, Geralyn Schad, Elizabeth Torello, Charine Tabbah, Philip Hamel, Hillary Feldman, Kara Palac, Rachel Mestel, Jordana Feto, Corrine Nawn, Kathryn Calicchio, Heather Flannery, Bruce Barton.
[1] Parkin TD, Clegg PD, French NP, Proudman CJ, Riggs CM, Singer ER, Webbon PM, Morgan KL. Risk of fatal distal limb fractures among Thoroughbreds involved in the five types of racing in the United Kingdom. Vet.Rec. 2004;154:493-497. [2] Sarrafian TL, Case JT, Kinde H, Daft BM, Read DH, Moore JD, Uzal FA, Stover SM. Fatal musculoskeletal injuries of Quarter Horse racehorses: 314 cases (1990-2007). J.Am.Vet.Med.Assoc. 2012;241:935-942. [3] Pool RR and Meagher DM. Pathologic findings and pathogenesis of racetrack injuries. Vet.Clin.North Am.Equine Pract. 1990;6:1-30. [4] Butcher MT, Hermanson JW, Ducharme NG, Mitchell LM, Soderholm LV, Bertram JE. Superficial digital flexor tendon lesions in racehorses as a sequela to muscle fatigue: a preliminary study. Equine Vet.J. 2007;39:540545. [5] Gerard MP and Hodgson DR. Equine Locomotion. In: Metabolic Energetics of Locomotion, Anonymous Metabolic Energetics of locomotion W.B. Saunders, 2001, pp. 327-349. [6] Johnston C, Gottlieb-Vedi M, Drevemo S, Roepstorff L. The kinematics of loading and fatigue in the standardbred trotter. Equine Vet.J.Suppl. 1999;(30):249-253. [7] Liederbach M, Schanfein L, Kremenic IJ. What is known about the effect of fatigue on injury occurrence among dancers? J.Dance Med.Sci. 2013;17:101-108. [8] Munsters CC, van Iwaarden A, van Weeren R, Sloet van OldruitenborghOosterbaan MM. Exercise testing in Warmblood sport horses under field conditions. Vet.J. 2014;202:11-19. [9] Schuback K and Essen-Gustavsson B. Muscle anaerobic response to a maximal treadmill exercise test in Standardbred trotters. Equine Vet.J. 1998;30:504-510. [10] Schuback K, Essen-Gustavsson B, Persson SG. Incremental treadmill exercise until onset of fatigue and its relationship to metabolic response and locomotion pattern. Equine Vet.J.Suppl. 1999;(30):337-341. [11] Eaton MD, Evans DL, Hodgson DR, Rose RJ. Effect of treadmill incline and speed on metabolic rate during exercise in thoroughbred horses. J.Appl.Physiol.(1985) 1995;79:951-957. [12] Astorino TA, Robergs RA, Ghiasvand F, Marks D, Burns S. Incidence of the oxygen plateau at VO2max during exercise testing to volitional fatigue
. Journal of Exercise Physiology Online 2000;3:1-12.
[13] Ratzlaff MH and Grant BD. The Use of Electrogoniometry and Cinematography in the Diagnosis and Evaluation of Forelimb Lameness. Proceedings of the annu conv of the Amer Assoc Equine Pract 1985;183-198. [14] Ratzlaff MH. Cinematography, Electrogoniometry, Thermography, and Dynamography. Equine Medicine and Surgery 1982;954-958. [15] Ratzlaff MH. The use of electrogoniometry to evaluate the effets of drugs on locomotion: A preliminary report. Proceedings of the Third International Symposium on Equine Medication Control 1979;397-419. [16] Taylor DPE, Tipton CM, Adrian M, Karpovich PV. Action of Certain Joints in the Legs of the Horse Recorded Electrogoniometrically. 1966;27:8589. [17] Ratzlaff MH. Relationship between locomotor forces, hoof position, and joint motion during the support phase of the stride of galloping horses. Acta Anatomica 1993;146:200-204. [18] Ratzlaff MH. Changes in digital venous pressures of horses moving at the walk and trot. American Journal of Veterinary Research 1985;46:1545-1549. [19] Adrian M, Grant BD, Ratzlaff MH, Ray J, Boulton C. Electrogoniometric Analysis of Equine Metacarpophalangeal joint Lameness. American Journal of Veterinary Research 1977;38:431-435. [20] Indramohan VP, Valsan G, Rowe PJ. Development and validation of a user-friendly data logger (SUDALS) for use with flexible electrogoniometers to measure joint movement in clinical trials. J.Med.Eng.Technol. 2009;33:650-655. [21] Bronner S, Agraharasamakulam S, Ojofeitimi S. Reliability and validity of a new ankle electrogoniometer. J.Med.Eng.Technol. 2010;34:350-355. [22] van der Linden ML, Andreopoulou G, Scopes J, Hooper JE, Mercer TH. Ankle Kinematics and Temporal Gait Characteristics over the Duration of a 6Minute Walk Test in People with Multiple Sclerosis Who Experience Foot Drop. Rehabil.Res.Pract. 2018;2018:1260852. [23] Dauncey T, Singh HP, Dias JJ. Electrogoniometer measurement and directional analysis of wrist angles and movements during the Sollerman hand function test. J.Hand Ther. 2017;30:328-336. [24] Colin A, Lequang P, Maitre P, Viguier E. Limbs electrogoniometric study in a healthy trotting dog. Computer methods in biomechanics and biomedical engineering 2008;61-62. [25] Gibert S, Carozzo C, Cachon T, Fau D, Genevois JP, Viguier E. Evaluation of the effectiveness of bandages on restricting carpus range of
motion in healthy dogs at a walk using electrogoniometry. Comput.Methods Biomech.Biomed.Engin. 2012;15 Suppl 1:140-142. [26] Drevemo S, Johnston C, Roepstorff L, Gustas P. Nerve block and intraarticular anasthesia of the forelimb in the sound horse. Equine Veterinary Journal (Suppl. 30), 266-269. Equine Vet.J.Suppl. 1999;266-269. [27] Clayton HM, Singleton WH, Lanovas JL, Prades M. Sagittal plane kinematics and kinetics of the pastern joint during the stance phase of the trot. Veterinary and comparative orthopaedics and traumatology : V.C.O.T 2002;15:15-17. [28] Van Weeren PR, van den Bogert AJ, Barneveld A. Correction models for skin displacement in equine kinematic gait analysis. Journal of Equine Veterinary Science 12, 178-192. Journal of Equine Veterinary Science 1992;12:178-192. [29] van den Bogert AJ, van Weeren PR, Schamhardt HC. Correction for skin displacement errors in movement analysis of the horse. J.Biomech. 1990;23:97-101. [30] Sha DH, Mullineaux DR, Clayton HM. Three-dimensional analysis of patterns of skin displacement over the equine radius. Equine Vet.J. 2004;36:665-670. [31] Clayton HM, Sha D, Stick J, Elvin N. 3D kinematics of the equine metacarpophalangeal joint at walk and trot. Vet.Comp.Orthop.Traumatol. 2007;20:86-91. [32] Childs BA, Pugliese BR, Carballo CT, Miranda DL, Brainerd EL, KirkerHead CA. Three-dimensional kinematics of the equine metacarpophalangeal joint using x-ray reconstruction of moving morphology - a pilot study. Vet.Comp.Orthop.Traumatol. 2017;30:248-255. [33] Clayton HM, Schamhardt HC, Willemen MA, Lanovaz JL, Colborne GR. Kinematics and ground reaction forces in horses with superficial digital flexor tendinitis. Am.J.Vet.Res. 2000;61:191-196. [34] Harrison SM, Whitton RC, Kawcak CE, Stover SM, Pandy MG. Relationship between muscle forces, joint loading and utilization of elastic strain energy in equine locomotion. J.Exp.Biol. 2010;213:3998-4009. [35] Herring M, Thompson K, Jarret S. Defining normal three-dimensional kinematics of the lower forelimb in horses. J of Equine Vet Science 1992;12:172-176. [36] Back W, Schamhardt HC, Barneveld A. Kinematic comparison of the leading and trailing fore- and hindlimbs at the canter. Equine Vet.J.Suppl. 1997;(23):80-83.
[37] Paavola M, Kannus P, Jarvinen TA, Khan K, Jozsa L, Jarvinen M. Achilles tendinopathy. J.Bone Joint Surg.Am. 2002;84-A:2062-2076. [38] Kannus P. Etiology and pathophysiology of chronic tendon disorders in sports. Scand.J.Med.Sci.Sports 1997;7:78-85. [39] Kellis E and Liassou C. The effect of selective muscle fatigue on sagittal lower limb kinematics and muscle activity during level running. J.Orthop.Sports Phys.Ther. 2009;39:210-220. [40] Chan-Roper M, Hunter I, W Myrer J, L Eggett D, K Seeley M. Kinematic changes during a marathon for fast and slow runners. J.Sports Sci.Med. 2012;11:77-82. [41] Hausswirth C, Bigard AX, Guezennec CY. Relationships between running mechanics and energy cost of running at the end of a triathlon and a marathon. Int.J.Sports Med. 1997;18:330-339. [42] Salgado E, Ribeiro F, Oliveira J. Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue. Knee 2015;22:243-248. [43] Granacher U, Gruber M, Forderer D, Strass D, Gollhofer A. Effects of ankle fatigue on functional reflex activity during gait perturbations in young and elderly men. Gait Posture 2010;32:107-112. [44] Christina KA, White SC, Gilchrist LA. Effect of localized muscle fatigue on vertical ground reaction forces and ankle joint motion during running. Hum.Mov.Sci. 2001;20:257-276. [45] Higham TE and Biewener AA. Fatigue alters in vivo function within and between limb muscles during locomotion. Proc.Biol.Sci. 2009;276:11931197. [46] Wickler SJ, Greene HM, Egan K, Astudillo A, Dutto DJ, Hoyt DF. Stride parameters and hindlimb length in horses fatigued on a treadmill and at an endurance ride. Equine Vet.J.Suppl. 2006;(36):60-64. [47] Mizrahi J, Verbitsky O, Isakov E, Daily D. Effect of fatigue on leg kinematics and impact acceleration in long distance running. Human Movement Science 2000;19:139-151. [48] Persson SG, Essen-Gustavsson B, Lindholm A. Energy profile and locomotor pattern of trotting on an inclined treadmill. Equine Exerc. Physiol. 1991;3:231-238. [49] McGuigan MP and Wilson AM. The effect of gait and digital flexor muscle activation on limb compliance in the forelimb of the horse Equus caballus. J.Exp.Biol. 2003;206:1325-1336.
[50] Walker VA, Walters JM, Griffith L, Murray RC. The effect of collection and extension on tarsal flexion and fetlock extension at trot. Equine Vet.J. 2013;45:245-248. [51] Birch HL, Wilson AM, Goodship AE. The effect of exercise-induced localised hyperthermia on tendon cell survival. J.Exp.Biol. 1997;200:17031708. [52] Back W, Barneveld A, Schamhardt HC, Bruin G, Hartman W. Longitudinal development of the kinematics of 4-,10-, 18-, and 26-month-old Dutch Warmblood horses. Equine Vet.J.Suppl. 1994;3-6. [53] Back W, Schamhardt HC, Van Weeren PR, Barneveld A. A comparison between the trot of pony and horse foals to characterize equine locomotion at young age. Equine Vet.J.Suppl. 1999;(30):240-244. [54] Clayton HM. The extended canter: a comparison of some kinematic variables in horses trained for dressage and for racing. Acta Anat.(Basel) 1993;146:183-187. [55] Holmstrom M, Magnusson LE, Philipsson J. Variation in conformation of Swedish warmblood horses and conformational characteristics of elite sport horses. Equine Vet.J. 1990;22:186-193. [56] van Weeren PR, van den Bogert AJ, Back W, Bruin G, Barneveld A. Kinematics of the standardbred trotter measured at 6, 7, 8 and 9 m/s on a treadmill, before and after 5 months of prerace training. Acta Anat.(Basel) 1993;146:154-161. [57] Smith RK and Webbon PM. Harnessing the stem cell for the treatment of tendon injuries: heralding a new dawn? Br.J.Sports Med. 2005;39:582-584. [58] Dowling BA and Dart AJ. Mechanical and functional properties of the equine superficial digital flexor tendon. Vet.J. 2005;170:184-192. [59] Bramlage L. Part I: Operative Orthopedics of the Fetlock Joint of the Horse: Traumatic and Developmental Diseases of the Equine Fetlock Joint. AAEP Proceedings 2009;55:96-143. [60] Schnabel LV and Redding WR. Diagnosis and management of proximal sesamoid bone fracture in the horse. Equine Veterinary Education 2018;30:450-455. [61] Janes JG, Kennedy LA, Garrett KS, Engiles JB. Common lesions of the distal end of the third metacarpal/metatarsal bone in racehorse catastrophic breakdown injuries. Journal of Veterinary Diagnostic Investigation 2017;29:431-436.
[62] Leach DH and Dyson S. Instant centres of rotation of equine limb joints and their relationship to standard skin marker locations. Equine Vet.J.Suppl. 1988;(6):113-119.
Figure Legends 1. Figure 1a and 1b; Electrogoniometer positioning: Latero-medial radiographs of the MCPJ in extension (Figure 1a) and flexion (Figure 1b) with dorsally affixed electrogoniometers (arrows). 2. Figure 2; Metacarpophalangeal joint (MCPJ) angle definition: The zero degree point is used as the reference to define positive and negative angles, and is the single line of best fit drawn parallel to the long axis of the third metacarpal bone (MCIII) and the first phalanx (P1) and passing through the MCPJ center of rotation (COR). This was found by determining the center of the distal condyles of MCIII [62]. The ϕ angles are positive and correspond with MCPJ extension. The ω angles are negative and refer to the MCPJ flexion angles. 3. Figure 3; Heart rate and blood lactate with onset of fatigue: Mean ± SD heart rate (beats per minute/bpm) and mean ± SD blood lactate (millimols per liter/mmol/L) measured for each gait during five treadmill events in which the horse was exercised to fatigue.
Table Legends 1. Table 1: Calculated mean, standard deviation (SD), and reproducibility coefficient for the difference between fluoroscopy- and electrogoniometry-derived angles (degrees) upon 6 calibrations of the electrogoniometers for each of three application methods: i. free coil, ii. Stockinette coil, and iii. tunnel coil. 2. Table 2: Effect of fatigue on kinematic values in a single horse by gait (trot 10.7 kph; slow canter: 21.5 kph; and fast canter: 35.1 kph) and limb. The horse always cantered on
the left lead with the “lead limb” referring to the horse’s left foreleg and the “non-lead limb” referring to the right foreleg. Angular velocity was measured only in the lead (left) foreleg. 3. Table 3: Effect of fatigue on temporal values in a single horse by gait (trot 10.7 kph; slow canter: 21.5 kph; and fast canter: 35.1 kph), measured from the lead limb. The horse always cantered on the left lead with the “lead limb” referring to the horse’s left foreleg and the “non-lead limb” referring to the right foreleg.
FUNDING: This work was supported by the National Center for Research Resources and the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health through Grant Number T32 OD011165; and Horsepower Technologies, Inc. Lawrence, MA, USA.
The sponsors had no role in study design; the collection, analysis or interpretation of data; in writing of the report; nor in the decision to submit the article for publication.
Manufacturers’ Addresses
i
150MM, SG150Bs by BIOPAC Systems Inc., Goleta, CA, USA
ii
DA100, BIOPAC Systems Inc., Goleta, CA, USA
iii
Elastikon (2” width), Johnson & Johnson, New Brunswick, NJ, USA
iv
General Electric Company OEC 9800 Plus, Fairfield, CT, USA
v
Patient Archiving and Communication System – Carestream Vue Version 11.4, Rochester, NY, USA vi
Equigym LLC, Lexington KY, USA
vii
Velcro Cable Ties, Velcro USA, Inc., Somersworth, NH, USA
viii
AcqKnowledge ACK100W by BIOPAC Systems Inc., Goleta, CA, USA
ix
78352A, Hewlett Packard, Boeblingen, Baden-Württemberg, DEU
x
Lactate Plus, Nova Biomedical, Waltham, MA, USA
xi
MILACATH Extended Use 14 Ga x 13 cm Radiopaque Polyurethane Catheter-over-
needle, Florence, KY, USA
Table 1: Calculated mean, standard deviation (SD), and reproducibility coefficient for the difference between fluoroscopy- and electrogoniometry-derived angles (degrees) upon 6 calibrations of the electrogoniometers for each of three application methods: i. free coil, ii. Stockinette coil, and iii. tunnel coil. In Vitro Metacarpophalangel Joint Angle (degrees) i. Free Coil ii. Stockinette iii. Tunnel Coil 1 Mean 2.14 2.38 2.87* 1 Standard Deviation 0.91 1.06 1.13 Reproducibility coefficient 1.83 2.11 * Indicates a significant difference (p<0.05) between the fluoroscopy-derived angles and the electrogoniometry derived angles. 1 n = 6. The average differences between the angles derived from the fluoroscopy unit and electrogoniometry hardware were used to compute the mean difference per calibration (6 calibrations); the mean and SD of these differences was then reported per treatment group.
Table 2: Effect of fatigue on kinematic values in a single horse by gait (trot 10.7 kph; slow canter: 21.5 kph; and fast canter: 35.1 kph) and limb. The horse always cantered on the left lead with the “lead limb” referring to the horse’s left foreleg and the “non-lead limb” referring to the right foreleg. Angular velocity was measured only in the lead (left) foreleg.
Outcome
MCPJ Max Extension Angle (Degrees)
Gait/Limb
S.E.
p-value** Fatigue Diff
Trot Right Left Slow Canter Non-lead Lead Fast Canter Non-lead Lead
MCPJ Max Flexion Angle (Degrees)
Fatigue Diff (Yes-No) LS Means* 7.34 4.45
0.96 0.74
<0.0001 <0.0001
11.98 10.76
1.26 0.97
<0.0001 <0.0001
12.74 7.40
1.27 0.98
<0.0001 <0.0001
1.39 1.64
1.02 0.79
0.52 0.16
1.44 -2.32
0.97 0.74
0.44 0.01
7.41 -0.55
0.97 0.75
<0.0001 0.88
Trot Non-lead Lead Slow Canter Non-lead Lead Fast Canter Non-lead Lead
Max Extension Angular Velocity (deg/s)
Trot Slow Canter Fast Canter
521.91 60.40 -315.44
22.57 22.47 51.37
<0.0001 0.008 <0.0001
Max Flexion Angular Velocity (deg/s)
Trot Slow Canter Fast Canter
121.45 221.48 -54.20
8.56 8.02 40.99
<0.0001 <0.0001 0.19
Notes: Negative sign indicates that fatigued state had lower value than non-fatigued state. * Least-Squares Means (LS Means) estimate of the difference in the outcome between the fatigued – non-fatigued gait from a mixed effects model stratified by limb with gait and fatigue included in the model using an unstructured variance-covariance matrix. ** p-value is from a Tukey-type adjustment for multiple comparisons across all LS Means pair-wise comparisons.
Table 3: Effect of fatigue on temporal values in a single horse by gait (trot 10.7 kph; slow canter: 21.5 kph; and fast canter: 35.1 kph), measured from the lead limb. The horse always cantered on the left lead with the “lead limb” referring to the horse’s left foreleg and the “non-lead limb” referring to the right foreleg.
Outcome
Gait/Limb
S.E.
Trot Slow Canter Fast Canter
Fatigue Diff (Yes-No) LS Means* -2.10 -7.04 -8.21
0.15 0.21 0.21
p-value** Fatigue Diff <0.0001 <0.0001 <0.0001
Stride Frequency (min)
Stride Duration (ms)
Trot Slow Canter Fast Canter
18.42 39.88 37.39
1.27 1.09 0.92
<0.0001 <0.0001 <0.0001
Table R1 Summary Table of Coefficients of Variation by Outcome Summarized Across Side, Gait, Fatigue State, and Test
Outcome: MCPJ Max Extension Angle (Degrees) Analysis Variable: CV Lower 95% Upper 95% N Mean Std Dev Median Minimum Maximum CL for Mean CL for Mean 48 0.897
N
0.437
0.777
0.230
2.371
0.770
1.024
Outcome: MCPJ Max Flexion Angle (Degrees) Analysis Variable: CV Lower 95% Upper 95% Mean Std Dev Median Minimum Maximum CL for Mean CL for Mean
48 -13.961
11.424 -12.728
-71.580
-2.162
-17.278
-10.644
Outcome: Stride Duration (ms) Analysis Variable: CV Lower 95% Upper 95% N Mean Std Dev Median Minimum Maximum CL for Mean CL for Mean 30 1.399 0.563 1.368 0.501 2.819 1.189 1.609
Outcome: Max Extension Angular Velocity (Degrees) Analysis Variable: CV Lower 95% Upper 95% N Mean Std Dev Median Minimum Maximum CL for Mean CL for Mean 30 8.915 3.954 8.757 3.469 19.884 7.439 10.392
Outcome: Max Flexion Angular Velocity (Degrees) Analysis Variable: CV Lower 95% Upper 95% N Mean Std Dev Median Minimum Maximum CL for Mean CL for Mean 30 -4.608 1.975 -4.283 -11.997 -1.897 -5.345 -3.871
Monday, March 11, 2019 Re:
“Effect of fatigue on metacarpophalangeal joint kinematics – a single horse pilot study”
All research animal procedures described herein were approved by Tufts University’s Institutional Animal Care and Use Committee; protocol # G201117.
Carl Kirker-Head MA, Vet MB, MRCVS, DACVS, DECVS Marilyn M Simpson Professor Director, Orthopaedic Research Laboratory Tufts Cummings School of Veterinary Medicine
S0737-0806(19)30598-2
DOI:
https://doi.org/10.1016/j.jevs.2019.102849
Reference:
YJEVS 102849
To appear in:
Journal of Equine Veterinary Science
Received Date: 12 March 2019 Revised Date:
30 July 2019
Accepted Date: 7 November 2019
Please cite this article as: Pugliese BR, Carballo CT, Connolly KM, Mazan MR, Kirker-Head CA, Effect of fatigue on equine metacarpophalangeal joint kinematics – a single horse pilot study, Journal of Equine Veterinary Science (2019), doi: https://doi.org/10.1016/j.jevs.2019.102849. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Inc.
Original Research Effect of fatigue on equine metacarpophalangeal joint kinematics – a single horse pilot study
Brenna R. Pugliese, Cristina T. Carballo, Kevin M. Connolly, Melissa R. Mazan, Carl A. Kirker-Head
Orthopaedic Research Laboratory, Cummings School of Veterinary Medicine at Tufts University
Corresponding author: Carl Kirker-Head, MA, Vet MB, MRCVS, DACVS, DECVS Department of Clinical Sciences 200 Westborough Road North Grafton, MA 01536, USA Email: [email protected] Telephone: 508-839-7926 Fax: 508-839-7922
Author emails: B.R. Pugliese, [email protected]; C.C. Carballo, [email protected]; K.M. Connolly, [email protected]; M.R. Mazan, [email protected]
CONFLICT OF INTEREST STATEMENT Dr. Carl Kirker-Head has received financial remuneration as a consultant from the study sponsor HorsePower Technologies, Inc. (Lowell, MA, USA).
Highlights •
The treadmill exercise regimen consistently induced metabolic fatigue
•
Electrogoniometry successfully generated metacarpophalangeal joint kinematic data
•
Metacarpophalangeal joint extension angle increased with fatigue
•
Stride duration increased with fatigue
CRediT Author Statement Brenna R. Pugliese: Methodology, Validation, Formal Analysis, Investigation, Data Curation, Writing – Original Draft, Writing – Review & Editing, Visualization, Project Administration. Cristina T. Carballo: Conceptualization, Methodology, Validation, Investigation, Data Curation, Writing – Original Draft, Writing – Review & Editing, Project Administration. Kevin M. Connolly: Formal Analysis, Investigation, Data Curation, Writing – Review & Editing, Visualization. Melissa R. Mazan: Conceptualization, Methodology, Investigation, Writing – Review & Editing, Supervision. Carl A. Kirker-Head: Conceptualization, Methodology, Investigation, Writing – Original Draft, Writing – Review & Editing, Visualization, Supervision, Project Administration, Funding Acquisition.
Abstract The objective was to validate a scientific method for characterizing equine metacarpophalangeal joint (MCPJ) motion in the non-fatigued and fatigued states using a single horse at trot, slow canter, and fast canter. One healthy Thoroughbred gelding exercised on a treadmill to exhaustion [fatigued state] (heart rate >190 BPM and blood lactate >10 mmol/L) while bilateral MCPJ angular data were acquired using electrogoniometry. Blood lactate and heart rate reflected transition from non-fatigued to fatigued states with increasing exercise duration and treadmill speed. Electrogoniometry consistently demonstrated: increase in mean MCPJ maximum extension angle with onset of fatigue; altered extension and flexion angular velocities with onset of fatigue; and increasing stride duration and decreasing stride frequency with onset of fatigue. The method allowed a preliminary but comprehensive characterization of the dynamic relationship between MCPJ kinematics and fatigue, prompting the need for multisubject studies that may enhance our ability to moderate exercise-related distal limb injury in equine athletes.
Keywords: equine; metacarpophalangeal joint; kinematic; fatigue; electrogoniometry
1. Introduction
The horse is an accomplished athlete largely by virtue of a conformation evolved to enhance locomotor efficiency. Yet these musculoskeletal adaptations predispose to injury, particularly in the proximity of the metacarpophalangeal joint (MCPJ) where there is a higher incidence of traumatic and degenerative lesions than elsewhere in the body [1-3]. The propensity for injury is exacerbated by metabolic fatigue [4], a complex physiological response to exercise resulting in an inability to sustain constant activity level [5]. Clinical observation implies that fatigue can induce substantial MCPJ hyperextension, yet only one scientific study [6] performed in Standardbreds briefly reports that fatigue increased MCPJ maximum extension angle by 5° during the trot on a treadmill. That limited characterization of MCPJ kinematics in the fatigued horse substantially limits our understanding of how trauma may be a sequela of fatigue-related alterations in locomotor pattern: muscle fatigue decreases muscular force development and contraction velocity and adversely alters neural feedback [7] leading to potentially injurious kinematic gait changes. A more precise characterization of the relationship between MCPJ motion and fatigue across a range of gaits may eventually enhance our ability to moderate exercise-related injury. This pilot study had several objectives: to validate a scientific method, specifically a treadmill exercise regimen as a means of inducing metabolic fatigue and electrogoniometry as a means of measuring equine MCPJ motion; further, we sought to comprehensively characterize sagittal plane MCPJ motion and temporal values at the trot, slow canter, and fast canter in this single horse in the non-fatigued and fatigued states, all as a prelude to conducting similar studies using a greater number of subjects.
2. Materials and Methods
2.1 In vitro data acquisition and technique validation 2.1.1
Animal. A single fresh equine cadaver distal forelimb, transected at mid-radius, was
harvested from an adult horse (~450 kg) euthanized at the Cummings School of Veterinary Medicine for reasons other than orthopedic pathology. To prepare the limb for testing, transection of the suspensory ligament, deep digital flexor tendon, and superficial digital flexor tendon was completed at mid-metacarpal III (MCIII) level to increase the available range of MCPJ motion (ROM) (81 degrees). The limb was positioned in lateral recumbency with the segment proximal to the MCPJ firmly immobilized. The segment of the limb distal to the MCPJ was allowed unrestricted movement in the sagittal plane (extension and flexion). 2.1.2
Instrumentation. A single 150-mm type electrogoniometeri and general-purpose
amplifierii were used to collect angular data onto a laptop computer. In every case, the electrogoniometer endblocks were secured to the limb using circumferentially applied elastic tapeiii like that subsequently used in vivo (see section 2.2.2 to follow). Three fixation methods were evaluated: i. Free coil - The hard plastic endblocks were secured to the limb but the flexible coil remained free; ii. Stockinette coil - As for ‘i’ above but the entire unit was additionally placed under a snug stockinette sock; and iii. Tunneled coil - As for ‘i’ above but the coil was additionally placed in a thin, soft fabric tunnel. 2.1.3
Imaging and signal calibration method. A fluoroscopy unitiv was placed perpendicular
to the cadaver limb and centered over the MCPJ to capture latero-medial images of the MCPJ at angles spanning from maximum extension to maximum flexion. The angles derived from the fluoroscopic images were subsequently used in a two-point calibration system to transform the simultaneously-derived electrical data collected from the electrogoniometers into degree units.
Medical imaging softwarev was used to measure the MCPJ angle from the fluoroscopic images. Using the Measurement software tool, a circle was overlaid on the condyle of distal MCIII, and the center of this circle was determined to be the MCPJ center of rotation (COR, MCPJ-COR). Lines were drawn from the mid-shaft of MCIII to the MCPJ-COR and again from the MCPJCOR to the mid-shaft of the distal first phalanx (P1). The angle between the two lines, as measured using the Markup Angle software tool, was subtracted from 180 to obtain the MCPJ angle. 2.1.4
Validation experiment. For each fixation method, the electrogoniometers were calibrated
6 times and on each occasion, 3 electrogoniometer-derived angles were determined (18 angles in total per treatment, except in treatment ii, where there were only 17 data points). The 3 angles recorded for the MCPJ for each fixation method corresponded to the maximum extension angle, the maximum flexion angle and a neutral angle between both extremes. For each of the 3 angular positions, MCPJ angle was derived concurrently from the electrogoniometer and from the fluoroscopic image. 2.1.5
Statistical analysis. The mean and standard deviation of the difference in angles
recorded by each modality (electrogoniometer and fluoroscopy) upon each calibration (n=6 per treatment group) was reported in this study to reflect the accuracy and repeatability of the electrogoniometer system as it reports MCPJ angle. To further characterize the method agreement, Paired t-tests were used to compare the angles obtained from the fluoroscopy unit with those obtained from the electrogoniometer for each fixation method. For the treatments where there was no statistical difference (p>0.05), indicating that there was no evidence of a systematic difference or bias, the coefficient of reliability was calculated to investigate the agreement between the fluoroscopy and electrogoniometry derived angles.
2.2 In vivo data acquisition 2.2.1
Animal. One healthy ‘off-the-track’ Thoroughbred gelding (6 years, 540±30 kg, 164 cm
at the withers) was used in all procedures approved by Tufts University’s Institutional Animal Care and Use Committee. The animal entered the program ‘racing fit’ two months prior to testing, during which time it acclimated to high-speed treadmillvi exercise five times weekly to maintain fitness. 2.2.2
Instrumentation. 150 mm single axis electrogoniometersi transformed the angular
position of the MCPJ in the sagittal plane (extension and flexion) into a proportional electrical signal with a sampling rate of 2000 Hz. The electrogoniometers were bilaterally affixed to the dorsal aspect of the MCPJ using circumferentially applied elastic tapeiii to secure the endblocks to mid-MCIII and to distal P1, respectively (free coil fixation method as in (i) above). The flexible coil spanned only the MCPJ. The proximal endblock was attached to a 3-meter-long extension cable directly connected to a general-purpose amplifierii, which allowed for augmentation of the electrical signal recorded by the laptop computer. The extension cable was affixed to the distal antebrachium using circumferentially applied elastic tape, and it was dorsally secured to the saddle using hook and loop fastenersvii. 2.2.3
Intra-session signal calibration method. Two latero-medial radiographs were taken of
each MCPJ following electrogoniometer placement, one with the joint in extension and one with the joint in flexion (Fig. 1a and 1b). The technique described to measure MCPJ angle from fluoroscopic images (see section 2.1.3) was similarly employed to measure MCPJ angle from the radiographs of the standing horse’s limb in both positions. The MCPJ angles derived from the standing and flexed images were used in a two-point calibration to transform the data into
degree units, by in-putting these values in the electrogoniometer software’s calibration functionviii. Calibration was performed prior to commencement of each of the 5 events. 2.2.4
Definition of MCPJ Angle. MCPJ angle, as measured by electrogoniometry, corresponds
to the angle between the long axes of MCIII and P1 (Fig. 2). The zero-degree point is the single line of best fit drawn parallel to the long axis of MCIII and P1 and passing through the MCPJ center of rotation (COR) and is used as a reference; a positive angle describes extension while a negative angle describes flexion. Maximum extension angles (most positive) were derived from stance phase angular data. Maximum flexion angles were the minimum (most negative) angles registered during the swing phase. 2.2.5
Exercise regimen. Data were collected for 5 standardized events [5 separate testing days,
one test per day, one week apart]. Each test took the horse from the non-fatigued to fatigued state through a series of graduated gaits and speeds. A 28.1 kg saddle and pad were secured on the horse’s back to increase exercise intensity. Warm-up consisted of walking exercise for 5 minutes (6.0 kph) followed by trotting for 5 minutes (10.7 kph) at 0o incline. The treadmill was then inclined to 6o for data collection. There followed a 1 minute fast canter (35.1 kph), 1 minute slow canter (24.1 kph), and 1 minute trot (10.7 kph) sequence, each preceded by 5 minutes of walking (6.0 kph) to normalize parameters. This provided for acquisition of nonfatigued data. The horse was then maintained at a fast canter (35.1 kph) for 8 minutes as exhaustion (fatigue) visibly ensued before immediately returning to a slow canter (1 minute) and trot (1 minute). The latter 3 test speeds were completed in the fatigued state as confirmed by heart rate and blood lactate analysis. 2.2.6
Fatigue status assessment. Metabolic variables were assessed during the last 15 seconds
of each exercise segment. Heart rate (beats per minute/BPM) was measured using cardiac
telemetryix. Blood lactate (millimols per liter/ mmol/L) was simultaneously measuredx using blood drawn from the catheterizedxi right jugular vein. Fatigue was confirmed with a heart rate >190 BPM, a maximum whole blood lactate >10 mmol/L, and the need for the horse to receive verbal encouragement to maintain pace with the treadmill [8]. Reported mean ± standard deviation (SD) heart rate and lactate for each condition were calculated across the five independent testing events, each one week apart. 2.2.7
Data Processing. An MP150 Data Acquisition System and AcqKnowledge softwareviii,
were used to generate real time MCPJ angle (degrees) vs time (seconds/sec) graphs. 2.2.8
Data Analysis. Thirty consecutive strides were analyzed for trot, slow canter and fast
canter for the non-fatigued and the fatigued states in both forelimbs on each of the five testing days. The first thirty strides of the non-fatigued conditions, and the last thirty strides of the fatigued conditions were assessed. Reported mean data were calculated across five independent testing events for the left leg and across three independent testing events for the right leg (a result of electrogoniometric equipment failure on two occasions). The horse always cantered on the left lead with the “lead limb” referring to the horse’s left foreleg and the “non-lead limb” referring to the right foreleg. Reported kinematic and temporal variables include mean ± standard error (SE): MCPJ maximum extension and flexion angle (degrees, deg), maximum extension and flexion angular velocity (degrees per second, degrees/sec), stride duration (milliseconds, msec) and stride frequency (strides per minute, str/min). Increase (percent, %) of MCPJ extension angles in the fatigue state over non-fatigued extension values were calculated as (ⱷfatigued x 100/ⱷnon-fatigued). 2.2.9
MCPJ Angular Velocity. Angular data was duplicated and transformed using
AcqKnowledge Software; the resultant waveform described angular velocity (deg/sec). The
maximum extension angular velocity (positive value) reported in this study corresponded to the maximum MCPJ velocity as it extended in stance phase. The maximum flexion angular velocity reported is the minimum (most negative) MCPJ velocity as it flexed in swing phase. 2.2.10 Stride Duration and Stride Frequency. Stride duration (ms) was calculated as time from one maximum extension angle to the next. Stride frequency was calculated as strides per minute (str/min). 2.2.11 Statistical analysis. To model these outcomes and adjust for the correlation among strides for each test, a mixed effects model was used for each outcome with limb/side, gait, fatigue state, and test as the predictors. A compound symmetry variance-covariance matrix was assumed and generated the least-squares (LS) means for each outcome to test the difference between the fatigued vs. non-fatigued state within limb/side and gait. Because LS means are derived statistics that tend to be normally distributed, a t-test was used to compare the LS means as above, as well as a Tukey adjustment for multiple comparisons. The standard calculation was used for the coefficient of variation within each limb, gait, fatigue state, and test to demonstrate the consistency of the measurements and of the variability. Metabolic data (heart rate and whole blood lactate) were compared in this single horse using descriptive statistics.
3. Results
3.1 In vitro data acquisition and technique validation Differences between pairs of MCPJ angles derived from i) fluoroscopic still images (regarded as the gold standard in this comparison) and ii) electrogoniometry were calculated and found to be normally distributed. The mean difference (in degrees) for each calibration (6 per treatment) was 2.14˚ for the free coil, 2.38˚ for the stockinette coil, and 2.87˚ for tunneled coil treatments (Table 1). There was a significant difference (P = 0.01) between the fluoroscopy-
derived angles and those derived using the electrogoniometer when the latter was applied to the limb using the tunneled coil technique. No significance was found between fluoroscopy-derived and electrogoniometry-derived measurements when using the free coil treatment (P = 0.25) or the stockinette coil treatment (P = 0.16). (Table 1). Since a significant difference between the angle calculation modalities in the free coil and stockinette coil treatments was not detected, the reproducibility coefficient (2 times the standard deviation of the differences) for these treatment groups was calculated to summarize the lack of agreement. The reproducibility coefficient for the mean difference within each set of angles and upon each calibration of the goniometers (n=6) was 1.83 for the free coil and 2.11 for the stockinette coil treatment (Table 1). The free coil was therefore selected as the most accurate and repeatable electrogoniometric technique and was subjected to further testing in vivo.
3.2 3.2.1
Metabolic Analysis The treadmill exercise regimen was well-accepted by the horse and consistently
prompted blood lactate values that reflected a transition from a non-fatigued state on completion of the initial one minute fast canter, slow canter and trot sequences, to a fatigued state [9, 10], starting as the horse progressed through the 8 minute fast canter and persisting through the end of the treadmill activity (fatigued trot) (Fig. 3). Mean ± SD blood lactate increased from 5.30 ± 1.24 mmol/L at the non-fatigued fast canter to 10.06 ± 3.10 mmol/L at the fatigued fast canter, continuing to rise during the subsequent transition from fatigued fast to slow canter (16.84 ± 2.44), reflecting a lag between fast canter exercise and the accompanying peak in lactate.
Lactate thereafter decreased during the fatigued trot (14.58 ± 1.85) though it remained well above baseline (1.38 ± 0.50) non-fatigued trot values. Mean ± SD heart rate (BPM) increased and decreased with increases and decreases in speed (Fig. 3). Heart rate was consistently elevated in the fatigued versus the non-fatigued states for the fast canter (201.6 ± 14.5 vs 170.8 ± 26.8), slow canter (180.33 ± 25.74 vs 158.80 ± 5.02), and trot (139.67 ± 8.14 vs 133.40 ± 20.77).
3.2.2
Kinematic Analysis The electrogoniometers required diligent preparation and placement to successfully
generate consistent data. Displacement of the goniometer under its adhesive tape eliminated right forelimb data in two of five trials. The kinematic data is reported in two formats: 1) Mean ± SE by gait, limb and fatigue status; and 2) quantitative difference between non-fatigued and fatigued data by gait and by limb (Tables 2 and 3). Lead (left) limb mean ± SE maximum extension angle (deg) consistently increased significantly (P < 0.0001) with fatigue at trot (60.15 ± 2.98 vs 64.60 ± 5.09), slow canter (71.49 ± 5.42 vs 82.83 ± 6.97), and fast canter (85.30 ± 6.49 vs 92.69 ± 8.46). Non-lead (right) limb mean ± SE maximum extension angle (deg) also increased significantly (P < 0.0001) with fatigue at trot (67.03 ± 2.29 vs 74.37 ± 2.97), slow canter (75.97 ± 1.77 vs 87.04 ± 3.59), and fast canter (75.98 ± 2.02 vs 88.72 ± 3.00). Fatigue did not produce consistent change (P>0.05) in mean ± SE maximum MCPJ flexion angles (deg) for trot (-26.92 ± 3.07 vs -25.28 ± 5.60) and fast canter (-35.35 ± 1.24 vs 35.89 ± 4.57) in the lead (left) limb, nor for trot (-22.46 ± 2.46 vs -21.07 ± 3.54) and slow canter
(-17.87 ± 1.66 vs -16.87 ± 3.14) in the non-lead (right) limb. However, in the lead limb fatigue prompted a significant (P=0.01) increase in maximum flexion angle at the slow canter (-26.35 ± 2.78 vs -28.18 ± 5.86). In the non-lead limb, fatigue significantly (P<0.0001) decreased MCPJ flexion angle at fast canter (-32.53 ± 1.29 vs -25.12 ± 2.43). With regard to angular velocity data, derived only from the lead limb, moderate changes were also noted with fatigue. For trot, fatigue prompted a significant (P < 0.0001) increase in mean ± SE maximum extension angular velocity (deg/sec) (1053.85 ± 37.37 vs 1577.29 ± 109.96) and corresponding significant (P < 0.0001) decrease in mean maximum flexion angular velocity (-1464.47 ± 51.54 vs -1343.16 ± 55.14). The pattern was repeated for slow canter, with mean maximum extension angular velocity significantly (P=0.008) increasing (1971.87 ± 60.39 vs 2032.53 ± 118.31) and mean maximum flexion angular velocity significantly (P < 0.0001) decreasing (-1940.80 ± 42.30 vs -1719.49 ± 52.34) with fatigue. At the fast canter, significant differences in angular velocity persisted but fatigue prompted a reversal in the direction of change with mean maximum extension velocity significantly (P < 0.0001) decreasing from 4879.54 ± 700.56 in the non-fatigued state to 4565.95 ± 547.07 in the fatigued state. Mean maximum flexion angular velocity did not significantly change with onset of fatigue at the fast canter (P=0.19).
3.2.3
Temporal Analysis Fatigue significantly (P<0.0001) increased mean ± SE stride duration (ms) at trot
(716.73 ± 3.23 vs 735.15 ± 0.91), slow canter (563.98 ± 1.33 vs 603.75 ± 1.21), and fast canter (504.55 ± 1.95 vs 541.96 ± 1.91). Fatigue significantly (P<0.0001) decreased mean ± SE stride
frequency at the trot (83.72 ± 0.38 vs 81.62 ± 0.10), slow canter (106.39 ± 0.25 vs 99.38 ± 0.20), and fast canter (118.92 ± 0.46 vs 110.71 ± 0.39).
4. Discussion
The treadmill exercise regimen was well tolerated by the horse and the regimen generated consistent data that confirmed the onset of fatigue, allowing correlation of metabolic state to MCPJ kinematics and temporal values. Increased blood lactate and heart rate parameters were consistent with values from previous reports of horses transitioning from a non-fatigued to fatigued state. The increase in lactate concentration with speed reported in this study has been previously documented [9-11] and, in this regard, the maximum mean whole blood lactate concentration reported during the fatigued canter (16.84 mmol/L) is consistent with previously published plasma lactate data (20.5 mmol/L) [10], recognizing that whole blood lactate corresponds to approximately 70% of plasma lactate values (0.7*20.5 mmol/L = 14.35 mmol/L). The increase in heart rate with speed of locomotion reported herein has also been previously described [9, 11], and the mean peak heart rate of 201.6 BPM during the fatigued fast canter is comparable to 212 BPM reported by Schuback et al. [10]. Subjectively, the onset of fatigue in this study was also characterized by the horse requiring verbal encouragement to keep pace with the treadmill [8], similar to human exercise studies in which volitional fatigue is the usual endpoint of an exercise test with considerable verbal encouragement being given to the subject [12]. Electrogoniometry is uncommonly applied in the horse and only 3 different authors report its use in characterizing MCPJ motion [13-19]. However, flexible electrogoniometry is widely accepted as a means of reliably collecting kinematic and temporal data across a range of functional activities in humans [20, 21]. Electrogoniometry has been validated in both the
human ankle [22] and wrist [23] as an accurate and cost-effective method for the clinical researcher as recently as 2018. Similar studies in canines have identified electrogoniometry as a suitable and sensitive instrument for measurement of joint angle in the distal limb [24, 25]. Though more complex modalities such as high-speed videography and marker-based motion analysis systems are widely available, we inferred from studies in human patients [22] that flexible electrogoniometry could provide the equine researcher with a more practical and financially affordable method to collect and interpret data. Hence, a cadaver limb validation of the BIOPAC electrogoniometer system was performed to determine the optimal method of MCPJ application as well as the accuracy of this method in the equine subject. This in vitro phase preceded live horse testing and evaluated the agreement between data obtained from each of 3 methods of electrogoniometer application (free coil, stockinette coil, tunneled coil) and a fluoroscopic method of angle analysis. The mean of the differences for each treatment represents a measure of accuracy, or how closely the angles derived from the electrogoniometers are to the real angles (as measured by the fluoroscopy unit), and the reproducibility coefficient is a measure of repeatability of the treatments. The free coil method of electrogoniometer attachment to the skin was the most accurate: average deviation from the true angle was 2.14°. This finding is similar to the accuracy of ±2˚ reported by the manufacturer. It was also the most repeatable as 95% of the differences fell within 1.83° of the mean difference (reproducibility coefficient). The free coil technique outperformed the stockinette coil method in both accuracy (2.14 vs 2.38) and repeatability (1.83 vs 2.11) and was therefore selected for in vivo testing. The tunnel coil method was the only treatment with a significant difference (p<0.05) between the electrogoniometer- and fluoroscopy-derived angles.
Consequently, the stockinette and tunnel methods described herein should not be used for equine MCPJ motion analyses in future studies. In the current study, the in vivo system employing the free coil method generated repeatable data but set-up required diligence and attention to detail. Even so, displacement of the goniometer under its elastic tape excluded right forelimb data in two of five trials. In subsequent studies, affixation of the end-blocks to the limb using additional means such as cyanoacrylate adhesive of the block to the hair coat could be considered. With skin-secured kinematic systems, it is always important to consider the potential effect of relative skin movement on the measurement of joint angle. Skin displacement might otherwise result in data variability and joint movement has been reported to be overestimated due to the associated soft tissue artifact [26-28]. To correct for this discrepancy, several models have been applied [28-30] while other researchers have resorted to using bone-fixed marker techniques [31, 32]. Fortunately, skin displacement below the carpus is negligible, and does not significantly affect kinematic analysis of the distal limb [28]; therefore, skin movement was not controlled for in this study. When we compared our electrogoniometric data in the non-fatigued horse with that previously generated using skin marker systems, we noted a similar mean MCPJ maximum extension angle (deg) at trot (60.15 versus 57.7, 61, and 50.7) [33-35]. A review of the limited relevant MCPJ electrogoniometric data from previous publications, wherein Ratzlaff reports an extension angle of 51 degrees at the trot in the non-fatigued horse on a level surface [13], also implies the validity of our technique. In the lead limb at slow canter, we report a mean MCPJ maximum extension angle (71.49), within reasonable range of values reported by Back et al., 1997 and Herring et al., 1992 (59.0 and 56.8, respectively). In the non-lead limb, we report
75.97 degrees mean maximum extension, in general agreement with 62.4 degrees reported by Back et al. 1997 [36] given breed, conformational, speed, and treadmill incline differences between studies. Thus, MCPJ electrogoniometry yielded apparently valid kinematic data. The consistency of the values generated by electrogoniometry with accepted standard values derived from skin marker systems gives credence to our measurement technique. In this study, fatigue induced increases in MCPJ maximum extension angle at all gaits. The fatigued trot in this Thoroughbred prompted a mean increase (P<0.0001) in extension angle (4.45° left [lead] limb, 7.34° right [non-lead] limb) compared with the non-fatigued trot, in general agreement with the 5° increase briefly reported in Standardbred trotters [6]. We also report a fatigue-induced increase (P<0.0001) in maximum MCPJ extension angle for slow canter (+10.76° lead limb, +11.98° non-lead limb) and fast canter (+7.40° lead limb, +12.74° non-lead limb), representing a 7-15% increase over non-fatigued extension values as defined using our MCPJ angle measuring protocol (ⱷfatigued x 100/ⱷnon-fatigued). (Table 2) The pathophysiology of tendinopathy in the fatigued equine is likely similar to humans with alterations in proprioception, loss of muscle control, and increase in misstep predisposing to clinical injury. Human acute Achilles tendinopathy, for example, can be caused by overexertion and muscle fatigue [37] which reduces energy absorption by the musculotendinous unit. Resultantly, muscle no longer protects tendon from strain injury [38] and the forces on passive tissues increase [7]. Our increase in mean MCPJ maximum extension angle with fatigue implies an increased strain in one or more elements of the flexor apparatus and associated risk of overload-related tendinopathy and/or desmopathy. Our swing phase data demonstrated no consistent trend in the mean maximum flexion angle between non-fatigued and fatigued states. Review of the human literature reveals similar
variability in limb joint flexion angles in non-fatigued and fatigued human athletes [39-41]. Compromised proprioception and associated loss of limb control secondary to high intensity exercise may contribute to variability in joint flexion data and precipitate injury in both species [42]. In the horse studied here, fatigue consistently induced changes in MCPJ angular velocities. Similarly, in humans, fatigue-induced changes in maximum angular velocity of the ankle joint have been documented and fatigue of the muscles surrounding the ankle effects dynamic stability [43]. Fatigued muscle, which normally acts eccentrically during the stance phase, becomes impaired in its concentric contraction and ability to achieve appropriate joint angle at touchdown [44]. Hence, fatigue-induced changes in equine MCPJ angular velocity may similarly predispose to injury of the joint and regional soft tissue structures. Our horse traveling at constant treadmill speed increased stride duration and proportionally decreased stride frequency in response to fatigue, consistent with previous reports in the equine and human [6, 45-47]. Reduction in stride frequency with fatigue, demonstrated across species, indicates a shift from optimal stride rate to a more metabolically costly state [47]. Speed is the product of stride length and stride frequency [48], and so horses must increase their stride length to maintain pace with the treadmill. This requires a larger vertical impulse and, because peak force is directly related to MCPJ angle [49], a corresponding increase in MCPJ extension, as we documented. Moreover, Walker et al. 2013 suggest that the greater horizontal displacement (i.e. greater stride length) of the horse at extended gaits also produces greater retraction and protraction when compared to collection [50]. This requirement for altered limb trajectory possibly increases stance phase loading forces, and ultimately the propensity for injury. Any or all of the aforementioned mechanisms might contribute to fatigue-
related tendinopathy/desmopathy in the horse, with exercise-induced hyperthermia and intermittent ischemia exacerbating tendon matrix degeneration [51] and injury risk. It is clinically important to recognize that horses fatigued during treadmill exercise respond differently, biomechanically, to those on land. During endurance rides, horses substantially reduce their speed [46] with fatigue. In our study, as previously discussed, constant treadmill speed with a decrease in stride frequency would have necessitated an increase in stride length – a parameter we did not measure directly. Regardless, the effect of speed and/or stride length are difficult to study in isolation since they act together with other constituents such as loading time, duty factor (predictive of peak forces), and muscle activation. This single-horse study provides for the first time a detailed characterization of the relationship between equine fatigue, MCPJ kinematics, and temporal values, but it has limitations. Testing a single Thoroughbred yields data that may not be representative of populations with breed, gait, conformation, age, or training-related differences [52-56]. Our understanding of the effects of fatigue on MCPJ motion could therefore be enhanced in future studies by simultaneous measurement of stance time and/or duty factor [49], peak vertical ground reaction force, and stride length in a diverse population of horses.
5. Conclusions
We present a detailed analysis of sagittal plane MCPJ motion in a single Thoroughbred racehorse in non-fatigued and fatigued states. The exercise regimen successfully and repeatably induced a transition from non-fatigued to fatigued states, which was effectively confirmed using the metabolic testing methods. The increases in MCPJ extension with fatigue, consistently recorded using electrogoniometry, may have significant clinical implications because hyperextension of the MCPJ likely increases the peak strain on the flexor tendons and
suspensory apparatus, predisposing these structures to overloading, accumulated microdamage, and ultimate tissue rupture [57, 58]. Importantly, hyperextension can also lead to fracture of the proximodorsal aspect of P1, palmar metacarpal condyles, and/or proximal sesamoid bones [5961]. Hence, characterization of MCPJ kinematics and gait temporal values in this preliminary study contributes an initial understanding of the effect of fatigue on joint motion and the implications for distal limb injury. Studies using a larger number of subjects and an expanded series of parameters are now appropriate.
Acknowledgements Kathy Trout, Geralyn Schad, Elizabeth Torello, Charine Tabbah, Philip Hamel, Hillary Feldman, Kara Palac, Rachel Mestel, Jordana Feto, Corrine Nawn, Kathryn Calicchio, Heather Flannery, Bruce Barton.
[1] Parkin TD, Clegg PD, French NP, Proudman CJ, Riggs CM, Singer ER, Webbon PM, Morgan KL. Risk of fatal distal limb fractures among Thoroughbreds involved in the five types of racing in the United Kingdom. Vet.Rec. 2004;154:493-497. [2] Sarrafian TL, Case JT, Kinde H, Daft BM, Read DH, Moore JD, Uzal FA, Stover SM. Fatal musculoskeletal injuries of Quarter Horse racehorses: 314 cases (1990-2007). J.Am.Vet.Med.Assoc. 2012;241:935-942. [3] Pool RR and Meagher DM. Pathologic findings and pathogenesis of racetrack injuries. Vet.Clin.North Am.Equine Pract. 1990;6:1-30. [4] Butcher MT, Hermanson JW, Ducharme NG, Mitchell LM, Soderholm LV, Bertram JE. Superficial digital flexor tendon lesions in racehorses as a sequela to muscle fatigue: a preliminary study. Equine Vet.J. 2007;39:540545. [5] Gerard MP and Hodgson DR. Equine Locomotion. In: Metabolic Energetics of Locomotion, Anonymous Metabolic Energetics of locomotion W.B. Saunders, 2001, pp. 327-349. [6] Johnston C, Gottlieb-Vedi M, Drevemo S, Roepstorff L. The kinematics of loading and fatigue in the standardbred trotter. Equine Vet.J.Suppl. 1999;(30):249-253. [7] Liederbach M, Schanfein L, Kremenic IJ. What is known about the effect of fatigue on injury occurrence among dancers? J.Dance Med.Sci. 2013;17:101-108. [8] Munsters CC, van Iwaarden A, van Weeren R, Sloet van OldruitenborghOosterbaan MM. Exercise testing in Warmblood sport horses under field conditions. Vet.J. 2014;202:11-19. [9] Schuback K and Essen-Gustavsson B. Muscle anaerobic response to a maximal treadmill exercise test in Standardbred trotters. Equine Vet.J. 1998;30:504-510. [10] Schuback K, Essen-Gustavsson B, Persson SG. Incremental treadmill exercise until onset of fatigue and its relationship to metabolic response and locomotion pattern. Equine Vet.J.Suppl. 1999;(30):337-341. [11] Eaton MD, Evans DL, Hodgson DR, Rose RJ. Effect of treadmill incline and speed on metabolic rate during exercise in thoroughbred horses. J.Appl.Physiol.(1985) 1995;79:951-957. [12] Astorino TA, Robergs RA, Ghiasvand F, Marks D, Burns S. Incidence of the oxygen plateau at VO2max during exercise testing to volitional fatigue
. Journal of Exercise Physiology Online 2000;3:1-12.
[13] Ratzlaff MH and Grant BD. The Use of Electrogoniometry and Cinematography in the Diagnosis and Evaluation of Forelimb Lameness. Proceedings of the annu conv of the Amer Assoc Equine Pract 1985;183-198. [14] Ratzlaff MH. Cinematography, Electrogoniometry, Thermography, and Dynamography. Equine Medicine and Surgery 1982;954-958. [15] Ratzlaff MH. The use of electrogoniometry to evaluate the effets of drugs on locomotion: A preliminary report. Proceedings of the Third International Symposium on Equine Medication Control 1979;397-419. [16] Taylor DPE, Tipton CM, Adrian M, Karpovich PV. Action of Certain Joints in the Legs of the Horse Recorded Electrogoniometrically. 1966;27:8589. [17] Ratzlaff MH. Relationship between locomotor forces, hoof position, and joint motion during the support phase of the stride of galloping horses. Acta Anatomica 1993;146:200-204. [18] Ratzlaff MH. Changes in digital venous pressures of horses moving at the walk and trot. American Journal of Veterinary Research 1985;46:1545-1549. [19] Adrian M, Grant BD, Ratzlaff MH, Ray J, Boulton C. Electrogoniometric Analysis of Equine Metacarpophalangeal joint Lameness. American Journal of Veterinary Research 1977;38:431-435. [20] Indramohan VP, Valsan G, Rowe PJ. Development and validation of a user-friendly data logger (SUDALS) for use with flexible electrogoniometers to measure joint movement in clinical trials. J.Med.Eng.Technol. 2009;33:650-655. [21] Bronner S, Agraharasamakulam S, Ojofeitimi S. Reliability and validity of a new ankle electrogoniometer. J.Med.Eng.Technol. 2010;34:350-355. [22] van der Linden ML, Andreopoulou G, Scopes J, Hooper JE, Mercer TH. Ankle Kinematics and Temporal Gait Characteristics over the Duration of a 6Minute Walk Test in People with Multiple Sclerosis Who Experience Foot Drop. Rehabil.Res.Pract. 2018;2018:1260852. [23] Dauncey T, Singh HP, Dias JJ. Electrogoniometer measurement and directional analysis of wrist angles and movements during the Sollerman hand function test. J.Hand Ther. 2017;30:328-336. [24] Colin A, Lequang P, Maitre P, Viguier E. Limbs electrogoniometric study in a healthy trotting dog. Computer methods in biomechanics and biomedical engineering 2008;61-62. [25] Gibert S, Carozzo C, Cachon T, Fau D, Genevois JP, Viguier E. Evaluation of the effectiveness of bandages on restricting carpus range of
motion in healthy dogs at a walk using electrogoniometry. Comput.Methods Biomech.Biomed.Engin. 2012;15 Suppl 1:140-142. [26] Drevemo S, Johnston C, Roepstorff L, Gustas P. Nerve block and intraarticular anasthesia of the forelimb in the sound horse. Equine Veterinary Journal (Suppl. 30), 266-269. Equine Vet.J.Suppl. 1999;266-269. [27] Clayton HM, Singleton WH, Lanovas JL, Prades M. Sagittal plane kinematics and kinetics of the pastern joint during the stance phase of the trot. Veterinary and comparative orthopaedics and traumatology : V.C.O.T 2002;15:15-17. [28] Van Weeren PR, van den Bogert AJ, Barneveld A. Correction models for skin displacement in equine kinematic gait analysis. Journal of Equine Veterinary Science 12, 178-192. Journal of Equine Veterinary Science 1992;12:178-192. [29] van den Bogert AJ, van Weeren PR, Schamhardt HC. Correction for skin displacement errors in movement analysis of the horse. J.Biomech. 1990;23:97-101. [30] Sha DH, Mullineaux DR, Clayton HM. Three-dimensional analysis of patterns of skin displacement over the equine radius. Equine Vet.J. 2004;36:665-670. [31] Clayton HM, Sha D, Stick J, Elvin N. 3D kinematics of the equine metacarpophalangeal joint at walk and trot. Vet.Comp.Orthop.Traumatol. 2007;20:86-91. [32] Childs BA, Pugliese BR, Carballo CT, Miranda DL, Brainerd EL, KirkerHead CA. Three-dimensional kinematics of the equine metacarpophalangeal joint using x-ray reconstruction of moving morphology - a pilot study. Vet.Comp.Orthop.Traumatol. 2017;30:248-255. [33] Clayton HM, Schamhardt HC, Willemen MA, Lanovaz JL, Colborne GR. Kinematics and ground reaction forces in horses with superficial digital flexor tendinitis. Am.J.Vet.Res. 2000;61:191-196. [34] Harrison SM, Whitton RC, Kawcak CE, Stover SM, Pandy MG. Relationship between muscle forces, joint loading and utilization of elastic strain energy in equine locomotion. J.Exp.Biol. 2010;213:3998-4009. [35] Herring M, Thompson K, Jarret S. Defining normal three-dimensional kinematics of the lower forelimb in horses. J of Equine Vet Science 1992;12:172-176. [36] Back W, Schamhardt HC, Barneveld A. Kinematic comparison of the leading and trailing fore- and hindlimbs at the canter. Equine Vet.J.Suppl. 1997;(23):80-83.
[37] Paavola M, Kannus P, Jarvinen TA, Khan K, Jozsa L, Jarvinen M. Achilles tendinopathy. J.Bone Joint Surg.Am. 2002;84-A:2062-2076. [38] Kannus P. Etiology and pathophysiology of chronic tendon disorders in sports. Scand.J.Med.Sci.Sports 1997;7:78-85. [39] Kellis E and Liassou C. The effect of selective muscle fatigue on sagittal lower limb kinematics and muscle activity during level running. J.Orthop.Sports Phys.Ther. 2009;39:210-220. [40] Chan-Roper M, Hunter I, W Myrer J, L Eggett D, K Seeley M. Kinematic changes during a marathon for fast and slow runners. J.Sports Sci.Med. 2012;11:77-82. [41] Hausswirth C, Bigard AX, Guezennec CY. Relationships between running mechanics and energy cost of running at the end of a triathlon and a marathon. Int.J.Sports Med. 1997;18:330-339. [42] Salgado E, Ribeiro F, Oliveira J. Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue. Knee 2015;22:243-248. [43] Granacher U, Gruber M, Forderer D, Strass D, Gollhofer A. Effects of ankle fatigue on functional reflex activity during gait perturbations in young and elderly men. Gait Posture 2010;32:107-112. [44] Christina KA, White SC, Gilchrist LA. Effect of localized muscle fatigue on vertical ground reaction forces and ankle joint motion during running. Hum.Mov.Sci. 2001;20:257-276. [45] Higham TE and Biewener AA. Fatigue alters in vivo function within and between limb muscles during locomotion. Proc.Biol.Sci. 2009;276:11931197. [46] Wickler SJ, Greene HM, Egan K, Astudillo A, Dutto DJ, Hoyt DF. Stride parameters and hindlimb length in horses fatigued on a treadmill and at an endurance ride. Equine Vet.J.Suppl. 2006;(36):60-64. [47] Mizrahi J, Verbitsky O, Isakov E, Daily D. Effect of fatigue on leg kinematics and impact acceleration in long distance running. Human Movement Science 2000;19:139-151. [48] Persson SG, Essen-Gustavsson B, Lindholm A. Energy profile and locomotor pattern of trotting on an inclined treadmill. Equine Exerc. Physiol. 1991;3:231-238. [49] McGuigan MP and Wilson AM. The effect of gait and digital flexor muscle activation on limb compliance in the forelimb of the horse Equus caballus. J.Exp.Biol. 2003;206:1325-1336.
[50] Walker VA, Walters JM, Griffith L, Murray RC. The effect of collection and extension on tarsal flexion and fetlock extension at trot. Equine Vet.J. 2013;45:245-248. [51] Birch HL, Wilson AM, Goodship AE. The effect of exercise-induced localised hyperthermia on tendon cell survival. J.Exp.Biol. 1997;200:17031708. [52] Back W, Barneveld A, Schamhardt HC, Bruin G, Hartman W. Longitudinal development of the kinematics of 4-,10-, 18-, and 26-month-old Dutch Warmblood horses. Equine Vet.J.Suppl. 1994;3-6. [53] Back W, Schamhardt HC, Van Weeren PR, Barneveld A. A comparison between the trot of pony and horse foals to characterize equine locomotion at young age. Equine Vet.J.Suppl. 1999;(30):240-244. [54] Clayton HM. The extended canter: a comparison of some kinematic variables in horses trained for dressage and for racing. Acta Anat.(Basel) 1993;146:183-187. [55] Holmstrom M, Magnusson LE, Philipsson J. Variation in conformation of Swedish warmblood horses and conformational characteristics of elite sport horses. Equine Vet.J. 1990;22:186-193. [56] van Weeren PR, van den Bogert AJ, Back W, Bruin G, Barneveld A. Kinematics of the standardbred trotter measured at 6, 7, 8 and 9 m/s on a treadmill, before and after 5 months of prerace training. Acta Anat.(Basel) 1993;146:154-161. [57] Smith RK and Webbon PM. Harnessing the stem cell for the treatment of tendon injuries: heralding a new dawn? Br.J.Sports Med. 2005;39:582-584. [58] Dowling BA and Dart AJ. Mechanical and functional properties of the equine superficial digital flexor tendon. Vet.J. 2005;170:184-192. [59] Bramlage L. Part I: Operative Orthopedics of the Fetlock Joint of the Horse: Traumatic and Developmental Diseases of the Equine Fetlock Joint. AAEP Proceedings 2009;55:96-143. [60] Schnabel LV and Redding WR. Diagnosis and management of proximal sesamoid bone fracture in the horse. Equine Veterinary Education 2018;30:450-455. [61] Janes JG, Kennedy LA, Garrett KS, Engiles JB. Common lesions of the distal end of the third metacarpal/metatarsal bone in racehorse catastrophic breakdown injuries. Journal of Veterinary Diagnostic Investigation 2017;29:431-436.
[62] Leach DH and Dyson S. Instant centres of rotation of equine limb joints and their relationship to standard skin marker locations. Equine Vet.J.Suppl. 1988;(6):113-119.
Figure Legends 1. Figure 1a and 1b; Electrogoniometer positioning: Latero-medial radiographs of the MCPJ in extension (Figure 1a) and flexion (Figure 1b) with dorsally affixed electrogoniometers (arrows). 2. Figure 2; Metacarpophalangeal joint (MCPJ) angle definition: The zero degree point is used as the reference to define positive and negative angles, and is the single line of best fit drawn parallel to the long axis of the third metacarpal bone (MCIII) and the first phalanx (P1) and passing through the MCPJ center of rotation (COR). This was found by determining the center of the distal condyles of MCIII [62]. The ϕ angles are positive and correspond with MCPJ extension. The ω angles are negative and refer to the MCPJ flexion angles. 3. Figure 3; Heart rate and blood lactate with onset of fatigue: Mean ± SD heart rate (beats per minute/bpm) and mean ± SD blood lactate (millimols per liter/mmol/L) measured for each gait during five treadmill events in which the horse was exercised to fatigue.
Table Legends 1. Table 1: Calculated mean, standard deviation (SD), and reproducibility coefficient for the difference between fluoroscopy- and electrogoniometry-derived angles (degrees) upon 6 calibrations of the electrogoniometers for each of three application methods: i. free coil, ii. Stockinette coil, and iii. tunnel coil. 2. Table 2: Effect of fatigue on kinematic values in a single horse by gait (trot 10.7 kph; slow canter: 21.5 kph; and fast canter: 35.1 kph) and limb. The horse always cantered on
the left lead with the “lead limb” referring to the horse’s left foreleg and the “non-lead limb” referring to the right foreleg. Angular velocity was measured only in the lead (left) foreleg. 3. Table 3: Effect of fatigue on temporal values in a single horse by gait (trot 10.7 kph; slow canter: 21.5 kph; and fast canter: 35.1 kph), measured from the lead limb. The horse always cantered on the left lead with the “lead limb” referring to the horse’s left foreleg and the “non-lead limb” referring to the right foreleg.
FUNDING: This work was supported by the National Center for Research Resources and the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health through Grant Number T32 OD011165; and Horsepower Technologies, Inc. Lawrence, MA, USA.
The sponsors had no role in study design; the collection, analysis or interpretation of data; in writing of the report; nor in the decision to submit the article for publication.
Manufacturers’ Addresses
i
150MM, SG150Bs by BIOPAC Systems Inc., Goleta, CA, USA
ii
DA100, BIOPAC Systems Inc., Goleta, CA, USA
iii
Elastikon (2” width), Johnson & Johnson, New Brunswick, NJ, USA
iv
General Electric Company OEC 9800 Plus, Fairfield, CT, USA
v
Patient Archiving and Communication System – Carestream Vue Version 11.4, Rochester, NY, USA vi
Equigym LLC, Lexington KY, USA
vii
Velcro Cable Ties, Velcro USA, Inc., Somersworth, NH, USA
viii
AcqKnowledge ACK100W by BIOPAC Systems Inc., Goleta, CA, USA
ix
78352A, Hewlett Packard, Boeblingen, Baden-Württemberg, DEU
x
Lactate Plus, Nova Biomedical, Waltham, MA, USA
xi
MILACATH Extended Use 14 Ga x 13 cm Radiopaque Polyurethane Catheter-over-
needle, Florence, KY, USA
Table 1: Calculated mean, standard deviation (SD), and reproducibility coefficient for the difference between fluoroscopy- and electrogoniometry-derived angles (degrees) upon 6 calibrations of the electrogoniometers for each of three application methods: i. free coil, ii. Stockinette coil, and iii. tunnel coil. In Vitro Metacarpophalangel Joint Angle (degrees) i. Free Coil ii. Stockinette iii. Tunnel Coil 1 Mean 2.14 2.38 2.87* 1 Standard Deviation 0.91 1.06 1.13 Reproducibility coefficient 1.83 2.11 * Indicates a significant difference (p<0.05) between the fluoroscopy-derived angles and the electrogoniometry derived angles. 1 n = 6. The average differences between the angles derived from the fluoroscopy unit and electrogoniometry hardware were used to compute the mean difference per calibration (6 calibrations); the mean and SD of these differences was then reported per treatment group.
Table 2: Effect of fatigue on kinematic values in a single horse by gait (trot 10.7 kph; slow canter: 21.5 kph; and fast canter: 35.1 kph) and limb. The horse always cantered on the left lead with the “lead limb” referring to the horse’s left foreleg and the “non-lead limb” referring to the right foreleg. Angular velocity was measured only in the lead (left) foreleg.
Outcome
MCPJ Max Extension Angle (Degrees)
Gait/Limb
S.E.
p-value** Fatigue Diff
Trot Right Left Slow Canter Non-lead Lead Fast Canter Non-lead Lead
MCPJ Max Flexion Angle (Degrees)
Fatigue Diff (Yes-No) LS Means* 7.34 4.45
0.96 0.74
<0.0001 <0.0001
11.98 10.76
1.26 0.97
<0.0001 <0.0001
12.74 7.40
1.27 0.98
<0.0001 <0.0001
1.39 1.64
1.02 0.79
0.52 0.16
1.44 -2.32
0.97 0.74
0.44 0.01
7.41 -0.55
0.97 0.75
<0.0001 0.88
Trot Non-lead Lead Slow Canter Non-lead Lead Fast Canter Non-lead Lead
Max Extension Angular Velocity (deg/s)
Trot Slow Canter Fast Canter
521.91 60.40 -315.44
22.57 22.47 51.37
<0.0001 0.008 <0.0001
Max Flexion Angular Velocity (deg/s)
Trot Slow Canter Fast Canter
121.45 221.48 -54.20
8.56 8.02 40.99
<0.0001 <0.0001 0.19
Notes: Negative sign indicates that fatigued state had lower value than non-fatigued state. * Least-Squares Means (LS Means) estimate of the difference in the outcome between the fatigued – non-fatigued gait from a mixed effects model stratified by limb with gait and fatigue included in the model using an unstructured variance-covariance matrix. ** p-value is from a Tukey-type adjustment for multiple comparisons across all LS Means pair-wise comparisons.
Table 3: Effect of fatigue on temporal values in a single horse by gait (trot 10.7 kph; slow canter: 21.5 kph; and fast canter: 35.1 kph), measured from the lead limb. The horse always cantered on the left lead with the “lead limb” referring to the horse’s left foreleg and the “non-lead limb” referring to the right foreleg.
Outcome
Gait/Limb
S.E.
Trot Slow Canter Fast Canter
Fatigue Diff (Yes-No) LS Means* -2.10 -7.04 -8.21
0.15 0.21 0.21
p-value** Fatigue Diff <0.0001 <0.0001 <0.0001
Stride Frequency (min)
Stride Duration (ms)
Trot Slow Canter Fast Canter
18.42 39.88 37.39
1.27 1.09 0.92
<0.0001 <0.0001 <0.0001
Table R1 Summary Table of Coefficients of Variation by Outcome Summarized Across Side, Gait, Fatigue State, and Test
Outcome: MCPJ Max Extension Angle (Degrees) Analysis Variable: CV Lower 95% Upper 95% N Mean Std Dev Median Minimum Maximum CL for Mean CL for Mean 48 0.897
N
0.437
0.777
0.230
2.371
0.770
1.024
Outcome: MCPJ Max Flexion Angle (Degrees) Analysis Variable: CV Lower 95% Upper 95% Mean Std Dev Median Minimum Maximum CL for Mean CL for Mean
48 -13.961
11.424 -12.728
-71.580
-2.162
-17.278
-10.644
Outcome: Stride Duration (ms) Analysis Variable: CV Lower 95% Upper 95% N Mean Std Dev Median Minimum Maximum CL for Mean CL for Mean 30 1.399 0.563 1.368 0.501 2.819 1.189 1.609
Outcome: Max Extension Angular Velocity (Degrees) Analysis Variable: CV Lower 95% Upper 95% N Mean Std Dev Median Minimum Maximum CL for Mean CL for Mean 30 8.915 3.954 8.757 3.469 19.884 7.439 10.392
Outcome: Max Flexion Angular Velocity (Degrees) Analysis Variable: CV Lower 95% Upper 95% N Mean Std Dev Median Minimum Maximum CL for Mean CL for Mean 30 -4.608 1.975 -4.283 -11.997 -1.897 -5.345 -3.871
Monday, March 11, 2019 Re:
“Effect of fatigue on metacarpophalangeal joint kinematics – a single horse pilot study”
All research animal procedures described herein were approved by Tufts University’s Institutional Animal Care and Use Committee; protocol # G201117.
Carl Kirker-Head MA, Vet MB, MRCVS, DACVS, DECVS Marilyn M Simpson Professor Director, Orthopaedic Research Laboratory Tufts Cummings School of Veterinary Medicine