Joint disease has been defined as a complex imbalance in the homeostatic mechanisms of degradation and repair, with the inflammatory cascade playing a crucial role in the progressive catabolic process.1 Numerous intra-articular treatments have been used to affect pathological manifestations of joint disease in horses by decreasing the degree of inflammation within the affected articulation.2–4 However, little attention has been focused on the various forms of physical rehabilitation that could aid in modifying joint disease and its progression in horses.5 Rehabilitative approaches have become effective treatment options for reducing or limiting harmful compensatory gait abnormalities in humans.6,7 Rehabilitation programs that address osteoarthritis and musculoskeletal injuries in humans often incorporate some form of aquatic exercise. Water provides an effective medium for exercise that can increase joint mobility, promote physiologically normal motor patterns, increase muscle activation, diminish limb edema, and reduce the incidence of secondary musculoskeletal injuries attributable to a primary articular injury.8,9 The increased resistance and buoyancy inherent in aquatic exercise minimize weight-bearing stresses applied to affected limbs, with a subsequent reduction in joint instability.10–14 Therefore, aquatic therapy has been an effective method of rehabilitation for humans with osteoarthritis who have difficulty with weight-bearing-associated exercises.12–14 Exercise in a UWT is one of multiple therapeutic modalities available for the rehabilitation of horses with musculoskeletal injuries15; unfortunately, there is little or no scientific evidence of its effectiveness for the treatment of osteoarthritis and associated musculoskeletal impairments in horses.
A repeatable method for experimental induction of carpal joint osteoarthritis in horses has been developed for assessing articular pathophysiologic processes and the efficacy of various therapeutic modalities.3,16–18 Results for the postural sway portion of a study19 indicated that exercise in a UWT significantly improves static balance control in horses with carpal joint osteoarthritis, which is pivotal to initiating evidence-based support for the use of aquatic exercise in the management of joint disease in horses. The purpose of the study reported here was to quantify clinical, biomechanical, and articular effects of exercise in a UWT, compared with results for simulated hand walking, in horses with unilateral experimentally induced carpal joint osteoarthritis. We hypothesized that aquatic treatment for horses with carpal joint osteoarthritis would enhance neuromuscular function, reduce thoracic limb gait abnormalities associated with carpal joint pain and inflammation, and improve histologic characteristics of affected carpal joints, which would provide further objective support for the use of aquatic rehabilitation.
Materials and Methods
Horses
Sixteen healthy 2- to 5-year-old horses were used in the study. The horses had been used in a study19 as part of a larger project to investigate the effect of exercise in a UWT on postural control. The Colorado State University Institutional Animal Care and Use Committee approved the study protocol.
Horses were evaluated before inclusion in the present study; the evaluation included a lameness examination, assessment of body condition, range of motion (flexion) testing of the carpal joints, evaluation for the presence of effusion in middle carpal joints, and radiography of the carpal joints. Horses without abnormal findings were enrolled in the study. A minimum acclimatization period of 14 days was provided to condition the horses to exercise on a high-speed treadmill and UWT prior to data collection.
Experimental induction of osteoarthritis
Horses were anesthetized and routinely prepared for surgery. Bilateral arthroscopic surgery of the middle carpal joints was performed on each horse to ensure that there were no preexisting articular lesions. During this procedure, an OCF (a repeatable method for inducing mild osteoarthritis and low-grade lameness3,16–18) was created in 1 arbitrarily selected middle carpal joint, and a sham procedure was performed in the contralateral middle carpal joint (day 0). The surgical approach and procedures used have been described previously.20 Animal-care personnel assessed the horses daily; heart rate, respiratory rate, rectal temperature, and willingness to move within the stall (horses were housed individually in 3.7 × 3.7-m stalls) were recorded.
Standardized exercise was used to aid in the induction and progression of carpal joint osteoarthritis. Beginning on day 15 (15 days after creation of the OCF), all horses exercised (trotting at 4.4 m/s for 2 minutes, galloping at 8.8 m/s for 2 minutes, and trotting again at 4.4 m/s) on an overground treadmilla 5 d/wk for the duration of the study (10 weeks) to promote development of carpal joint osteoarthritis.
Treatments
One week after surgery (day 7), horses were ranked on the basis of lameness score and arbitrarily assigned to 1 of 2 groups21 (8 horses/group). The treatment group began exercising in a UWTb starting on day 15. The water level in the UWT was maintained at the tuberculum majus pars cranialis for the duration of the study, which provided approximately 60% reduction in weight bearing.22 Exercise in the UWT consisted of a brisk walk (2.1 m/s) for 5 minutes once a day for 5 days. At weekly intervals, duration of exercise in the UWT was increased by 5 minutes, until a maximum of 20 min/session was reached. Horses exercised for 20 minutes once a day, 5 d/wk, for the remainder of the 10-week study (ie, total exercise duration, 8 weeks). The control group exercised in the same UWTb but without the addition of water; exercise was at the same speed, frequency, and duration as for the treatment group, and it also started on day 15 for a total duration of 8 weeks. The low-speed exercise for the control group was intended to simulate hand walking and light exercise.
Gait experiments
The GRFs, thoracic limb kinematics, and EMG activity were recorded simultaneously for each horse at 4 time points during the study: before creation of the OCF (day -7 [baseline]), after creation of the OCF but prior to initiating control and treatment exercise (day 14), 4 weeks after starting exercise treatments (day 42), and at study conclusion (day 70). For data collection, horses were trotted by an experienced handler at a uniform velocity selected by each horse (2.8 to 3.4 m/s); trials were not accepted when velocity was greater than ± 10% of the mean baseline value for each horse. Forward velocity was measured with a series of 5 infrared emitters and corresponding reflective sensorsc placed 2 m apart. The initial ground contact and toe-off events for each step per 10-second trial were identified with a biaxial accelerometer adhered to the dorsolateral hoof wall of each of the front hooves. The initial hoof ground contact and toe (off) leaving the ground (stance phase) events were used to determine EMG timing of selected thoracic limb muscles during the stance and swing phases over a minimum of 4 strides. Kinetic, kinematic, and mean values for EMG temporal variables across 3 trials were calculated and then normalized on the basis of stride duration.
Kinetic analysis
The GRFs for all 4 limbs were recorded by use of 2 strain gauge-based force platformsd (60 × 90 cm) mounted sequentially in a concrete base in the center of a 25-m runway. The force platforms and runway were covered with a 9-mm-thick rubber mat to prevent horses from slipping during locomotion. Each horse was led by an experienced handler in a straight line over the runway and force platforms at a consistent trotting velocity. A kinetic trial was considered successful when ipsilateral thoracic and pelvic limb pairs contacted the center of a single force platform. Three valid trials were collected during each data session. Orthogonal GRF data were sampled at 3,000 Hz; however, only the vertical and craniocaudal GRFs were analyzed for this study. Kinetic parameters calculated for each trial were stance duration; peak vertical, braking, and propulsion forces and impulses; time to maximum vertical, braking, and propulsion forces; and vertical loading rates. Kinetic variables were normalized on the basis of body weight.
Kinematic analysis
Hair was clipped over the palpated centers of joint rotation, and the centers were marked with permanent red lacquer to ensure consistent marker placement throughout the study. Cyanoacrylate gluee was used to adhere 2.5-cm spherical retroreflective markers to the skin overlying anatomic landmarks23 on both thoracic limbs (Figure 1). Thoracic limb joint angles were calculated on the basis of the anatomic flexor surface of each joint. Additional markers were placed over the left and right transverse processes of the first cervical vertebra, dorsal midline of the frontal bones at the level of the supraorbital foramen, spinous process of the fifth thoracic vertebra, and tuber sacrale. Optical data were collected at 200 Hz by use of a motion-analysis systemf with 8 high-speed infrared camerasg distributed equally around the periphery of the force platforms. Capture volume over the region of the force platforms was calibrated by use of a customized calibration frame and wand with an accuracy of 0.7 mm. Raw coordinate data were filtered with a low-pass fourth-order recursive Butterworth filter at 12 Hz. Kinematic variables calculated for each trial included maximum and minimum joint angles during the stance and swing phases and time to peak joint angles during each stride.
Photograph of a representative horse depicting placement of retroreflective kinematic markers over the joint centers of rotation of the right thoracic limb, with additional markers located proximal to the shoulder joint placed over the dorsal one-third of the scapular spine and directly over the spinous process of T5. Notice the solid red line connecting the centers of joint rotation. The flexor surface for each joint is indicated (dashed red arcs), and the blue surface electrodes with corresponding cables are attached to the telemetry unit and affixed to the surcingle.
Citation: American Journal of Veterinary Research 78, 5; 10.2460/ajvr.78.5.558
EMG analysis
Prior to initiation of the present study, CVs were calculated to determine the reliability for use of the non-weight-bearing limb position to determine resting muscle EMG mean and SD values. The EMG data were collected over 2 consecutive days; 3 trials were collected for each forelimb. Once the CVs were determined, a 2-sample t test was used to determine whether a significant difference existed between values for day 1 and day 2. The EMG variables calculated for each trial included duration of muscle activity as well as timing of muscle activation and inactivation during each stride.
For the study reported here, surface and fine-wire EMG signals were collected simultaneously with the kinetic and kinematic data at the aforementioned time points from 7 muscles on the distal aspect of the forelimb (extensor carpi radialis, flexor carpi radialis, ulnaris lateralis, flexor carpi ulnaris, long head of the triceps brachii, SDF, and humeral head of the DDF muscles; Appendix) responsible for flexion-extension and stabilization of the carpus joint. Horses were sedated by IV administration of detomidine hydrochlorideh (0.01 mg/kg). Bipolar surface electrodesi were adhered with cyanoacrylate glue onto shaved cleaned skin overlying the midbody of the forelimb muscles of interest. Skin was prepared in a sterile manner, and 1 mL of lidocaine hydrochloride 2%j was injected SC with a 25-gauge, 5/8-inch needle. Stainless steel, 7-strand, polytetrafluoroethylene-coated, fine-wire electrodesk (the coating was stripped from 1 cm of each end of the electrodes) were fed through a 23-gauge, 1.5-inch needle for insertion into individual muscles. Ultrasound guidance was used to assist insertion of fine-wire electrodes (3 cm apart) into the midbody of the SDF and humeral head of the DDF muscles. A butterfly tab of athletic tape was placed around the portion of the fine-wire electrodes exterior to the skin, and the tape was anchored to the skin with a single simple interrupted suture24 of 3–0 poliglecaprone 25.l A ground surface electrode was placed over the skin on the proximal aspect of the radius. All EMG electrodes were connected to preamplified cables attached to a telemetry unitm that was secured to a surcingle (Figure 1). Collection of EMG data began after the horses had fully recovered from sedation (90 to 120 minutes after administration of sedative). Location of each surface electrode and the adjacent anatomic landmarks were traced onto clear acetate sheets to help improve repeatable electrode placement among data sessions. Insertion sites for the fine-wire electrodes in the SDF and humeral head of the DDF muscles were measured proximally from the accessory carpal bone, and the depth of insertion was measured ultrasonographically.
Differentiating the borders of the SDF muscle from the DDF muscle in the distal aspect of the radius was performed by use of a distal-to-proximal ultrasonographic approach. Identifying the borders of the tendinous portion of the SDF muscle in the proximal aspect of the metacarpus and following it proximally through the carpal canal makes the dorsal border of the SDF muscle and caudal border of the DDF muscle most apparent at the level of the distal aspect of the radius.25 The SDF muscle typically was best differentiated from the DDF muscle 6 to 9 cm proximal to the accessory carpal bone. This region was chosen because at more proximal locations, the SDF muscle may be indistinct from the adjacent DDF muscle.25 In addition, the humeral head of the DDF muscle is positioned more laterally at this location,25 which for stability and placement of the fine-wire electrodes was more amenable to maintaining the electrodes in place. The humeral head of the DDF muscle has long muscle fibers that operate over a long range of muscle lengths and therefore assists with carpal joint flexion in the swing phase of the gait.26 This is in contrast to the radial head and ulnar heads of the DDF muscle, which have shorter muscle fiber lengths and thus contribute to stability of the carpus joint during initial ground contact.26 Because the ulnaris lateralis and flexor carpi ulnaris muscles (both of which have short muscle fibers) stabilize the carpus during the stance phase, the purpose of measuring muscle activity for the humeral head of the DDF muscle was to determine potential changes during the swing phase of the gait.
Raw EMG data were collected at 3,000 Hz, filtered through a high-pass filter (120 Hz), zeromeaned, full-wave rectified, and filtered with a low-pass recursive fourth-order Butterworth filter (15 Hz). The EMG parameters of interest included muscle activation and deactivation (muscle on-off) timing and the duration of electrical activity within each muscle. To calculate threshold values needed for determination of the on-off timing of muscle activation, mean and SD values of EMG amplitude were calculated over 1 second for each muscle while it was least active during a non-weight-bearing limb position with the carpal joint slightly flexed. Threshold values for individual muscles were calculated from 2 to 8 SDs from resting EMG signals and used to define active (above threshold) and inactive (below threshold) muscle activity.27 A minimum 50-millisecond duration of persistent EMG activity above threshold was used to minimize the effect of a single spontaneous EMG spike triggering on-off timing of muscle activity. Threshold values calculated for each muscle at baseline were used to calculate on-off timing across all data sessions.
Lameness scores
Clinical examination and lameness examinations for both thoracic limbs were performed at day -7 and weekly thereafter throughout the study period. Horses were trotted on hard ground, and lameness simultaneously was graded by use of the American Association of Equine Practitioners’ lameness scale28 (scale, 0 [normal gait] to 5 [severe lameness]) by an experienced equine orthopedic surgeon (CEK) who was unaware of treatment group assignment for each horse.
Prolonged carpal joint flexion at end range of motion and repeated lameness evaluation during trotting was performed and graded on a scale of 0 to 4 (0 = no response, 1 = slight response, 2 = mild response, 3 = moderate response, and 4 = severe lameness response). Clinical lameness grades were published as part of a previous study19 because the improvements in subjective lameness scores for horses during UWT exercise corresponded with a significant improvement in postural sway variables. In that study,19 it was critical to demonstrate that although UWT exercise did not have a beneficial effect on lameness scores at all time points, improvements in balance control appear to translate into improved functional locomotion.
Goniometry
Prior to initiation of the present study, CVs were calculated to determine the reliability of goniometry for measurement of passive joint range of motion for the forelimbs. Intrarater reliability to assess forelimb joint angle measurements was performed by use of 3 horses that were measured weekly for 4 weeks. The CV was determined for each joint position (flexion and extension), and it was found that the CV for all measurements was ≤ 6%.
For the study reported here, data for joint passive range of motion were collected weekly for both thoracic limbs starting at baseline and continuing throughout the study. To provide repeatable anatomic placement of the goniometern between sessions, hair was removed with a No. 40 clipper blade over the joint centers of rotation,23 and the centers of rotation were permanently marked with red lacquer. Joints of interest included the shoulder, elbow, carpus, and metacarpophalangeal joints. The center of the goniometer was placed laterally over each joint center of rotation. To limit variability, the end of each arm of the goniometer was positioned over the proximal and distal centers of joint rotation, except when the proximal arm of the goniometer was aligned parallel to the spine of the scapula during assessment of the shoulder joint passive range of motion. Throughout the study, each articulation was held at the flexion and extension end ranges of motion by an experienced veterinarian (MRK) while joint angles were recorded by the same assistant. Three consecutive measurements of each joint angle were recorded, and the mean value was calculated.
Diagnostic imaging
Radiographic evaluations of both carpi were performed at day -7 (baseline data collection to confirm the absence of osseous pathological changes), day 14 (14 days after creation of the OCF to assess acute osseous changes), and day 70 (study conclusion to evaluate progression of osteoarthritis). A board-certified veterinary radiologist (NMW) who was unaware of the treatment group assignment graded the carpal radiographs for osseous proliferation at the dorsal joint capsule attachment of the radial carpal bone and for subchondral bone lysis, sclerosis, and osteophyte formation. Grades were assigned on a scale of 0 to 4 (0 = no detectable abnormality, 1 = slight change, 2 = mild change, 3 = moderate change, and 4 = severe change).
Histologic examination
Horses were euthanized at the end of the study. Samples of synovial membrane, fibrous joint capsule, and articular cartilage were harvested during necropsy, placed in neutral-buffered 10% formalin, and processed for histologic examination by an evaluator who was not aware of the source of the samples. Tissue sample locations, processing techniques, and lesion grading scales were based on methods described for the joint carpal OCF technique.29
Statistical analysis
Sample size calculations were based on effect sizes and variances previously reported by use of the OCF method in the equine carpus.2,3 Analysis (statistical power = 0.90 and α = 0.05) indicated that 16 horses were needed. Statistical softwareo was used to evaluate data by use of an ANOVA or ANCOVA framework, depending on the absence or presence of a covariate, respectively. The GRF and joint angle data were analyzed by use of baseline (day -7) data as a covariate to adjust for differences that existed at that time point. An ANOVA was used to determine significant main effects and interactions between main-effect variables. Independent main-effect variables were presence or absence of osteoarthritis, day of sample collection, and treatment group (exercise in a UWT and in a UWT without water [simulated hand walking]). The potential effect of horse on outcome variables was controlled with the introduction of a random effect for horse. Least squares means were used for individual comparisons. Residual plots were used to determine normality; all outcome parameters had a normal distribution. Values were reported as mean ± SEM, and values of P ≤ 0.05 were considered significant.
Results
Kinetics
The velocity of horses during gait analysis did not differ significantly on the basis of treatment group (P = 0.89) or day of data collection (P = 0.69). Within the pelvic limbs, there were no significant effects of OCF or treatment on any kinetic parameter. Within the thoracic limbs, stance duration for the OCF limbs differed significantly (P = 0.002) from that for the sham-operated limbs depending on whether the horse was in the UWT exercise or control group (Table 1). Within the control group, the OCF limb had a significantly increased stance duration, compared with stance duration for the contralateral sham-operated limb. In contrast, the OCF limb within the UWT exercise group had a significantly decreased stance duration, compared with the stance duration for the sham-operated limb.
Mean ± SEM values for GRF variables measured in the OCF and sham-operated limbs of horses in the UWT exercise group (n = 8) and control group (simulated hand walking; 8) over all sample collection periods.
| Treatment | |||
|---|---|---|---|
| Variable | Limb | Control | UWT |
| Stance duration (ms) | OCF | 315.0 ± 3.0 | 306.0 ± 3.0 |
| Sham | 311.0 ± 3.0* | 310.0 ± 3.0*† | |
| Peak vertical force (N/kg) | OCF | 10.0 ± 0.2 | 10.5 ± 0.2 |
| Sham | 11.0 ± 0.2* | 10.4 ± 0.2 | |
| Loading rate (N/ms) | OCF | 7.4 ± 0.3 | 7.7 ± 0.3 |
| Sham | 7.6 ± 0.3* | 7.6 ± 0.3 | |
Within a variable within a treatment, value differs significantly (P ≤ 0.05) from the value for the OCF limb.
Within a row, value differs significantly (P ≤ 0.05) from the value for the control treatment.
Peak vertical GRF differed significantly (P = 0.02) between OCF and sham-operated limbs depending on whether the horse was in the UWT exercise or control group. Comparisons within the control group revealed that OCF limbs had a decreased peak vertical GRF that differed significantly (P = 0.007) from that for the sham-operated limbs (Table 1). However, there were no significant differences between the OCF and sham-operated limbs within the UWT exercise group. Peak braking and propulsion forces, impulses, and time to peak forces within the thoracic limbs did not change significantly with OCF creation.
The vertical GRF loading rates within the OCF and sham-operated limbs differed significantly (P = 0.008) depending on treatment group. Within the control group, OCF limbs had a significantly reduced limb loading rate, compared with results for the sham-operated limbs (Table 1). There was no significant difference in loading rates between the OCF and sham-operated limbs for the UWT exercise group.
Kinematics
Joint kinematics was determined for the stance phase and swing phase of the stride.
Stance phase—The OCF limb had significantly (P = 0.002) increased shoulder joint extension during the stance phase of the stride (P = 0.002), compared with results for the sham-operated limb (Table 2). Type of exercise (UWT or control group) did not significantly influence shoulder joint extension. Mean ± SEM elbow joint extension in the OCF limb (150.0 ± 1.0°) was significantly (P = 0.01) increased in the UWT exercise group, compared with results for the control group (148.0 ± 1.0°). Depending on the study day, the percentage of stride duration during which peak carpal joint extension occurred was significantly influenced by the presence or absence of an OCF. Peak carpal joint extension of OCF limbs was detected significantly (P = 0.01) earlier on day 42 (25 ± 2%), compared with results for day 14 (31 ± 2%).
Mean ± SEM values for variables of thoracic limb joint angles measured in the OCF and sham-operated limbs (8 limbs/group) over all sample collection periods.
| Joint | Limb | Peak stance angle (°) | Peak swing angle (°) | Peak extension (% of stride) | Peak flexion (% of stride) |
|---|---|---|---|---|---|
| Shoulder | OCF | 128.0 ± 0.7 | 120.0 ± 0.5 | 2.85 ± 0.4 | 53.0 ± 1.2 |
| Sham | 125.0 ± 0.7* | 117.0 ± 0.5* | 2.44 ± 0.4 | 53.0 ± 1.2 | |
| Elbow | OCF | 149.0 ± 0.7 | 99.0 ± 0.5 | 46.0 ± 0.8 | 88.0 ± 0.7 |
| Sham | 148.0 ± 0.7 | 97.0 ± 0.5* | 47.0 ± 0.8 | 89.0 ± 0.7 | |
| Carpus | OCF | 177.0 ± 0.3 | 107.0 ± 1.0 | 28.0 ± 0.9 | 75.0 ± 1.0 |
| Sham | 176.0 ± 0.3 | 104.0 ± 1.0* | 29.0 ± 0.9 | 75.0 ± 1.0 | |
| Metacarpophalangeal | OCF | 249.0 ± 0.9 | 184.0 ± 0.2 | 30.0 ± 0.7 | 73.0 ± 1.2 |
| Sham | 249.0 ± 0.9 | 184.0 ± 0.2 | 31.0 ± 0.7 | 75.0 ± 1.2 |
Within a joint within a variable, value differs significantly (P ≤ 0.05) from the value for the OCF limb.
Swing phase—Creation of an OCF significantly (P = 0.002) decreased flexion for the shoulder joint, elbow joint, and carpal joint during the swing phase, compared with results for the sham-operated limb (Table 2). Type of exercise did not significantly influence shoulder joint, elbow joint, or carpal joint angles during the swing phase.
EMG
The CVs ranged from 2% (long head of the triceps brachii muscle) to 38% (humeral head of the DDF muscle) for each of the 7 selected muscles. The CV for the other muscles was 6% for the flexor carpi ulnaris muscle, 7% for the flexor carpi radialis and ulnaris lateralis muscles, 13% for the extensor carpi radialis muscle, and 32% for the SDF. There were no significant differences detected between the 2 consecutive days.
Creation of an OCF significantly affected the onset of muscle activity for the ulnaris lateralis and DDF muscles (Table 3). A significant treatment effect was found in onset of muscle activation for the ulnaris lateralis muscle.
Mean ± SEM values for EMG parameters for each muscle in the OCF and sham-operated thoracic limbs (8 limbs/group).
| Muscle | Limb | Activation onset (% of stride) | Activation termination (% of stride) | Duration of activity (% of stride) | Duration of activation (ms) |
|---|---|---|---|---|---|
| Extensor carpi radialis | OCF | 64.0 ± 1.1 | 83.0 ± 1.0 | 20.0 ± 1.1 | 133.0 ± 7.4 |
| Sham | 64.0 ± 1.1 | 83.0 ± 1.0 | 19.0 ± 1.1 | 134.0 ± 7.4 | |
| Ulnaris lateralis | OCF | 91.0 ± 0.8 | 35.0 ± 1.3 | 45.0 ± 1.3 | 307.0 ± 10.1 |
| Sham | 89.0 ± 0.8* | 36.0 ± 1.3 | 46.0 ± 1.3 | 314.0 ± 10.1 | |
| Flexor carpi radialis 1† | OCF | 10.0 ± 0.94 | 29.0 ± 1.7 | 19.0 ± 1.5 | 126.0 ± 10.2 |
| Sham | 9.0 ± 0.94 | 28.0 ± 1.7 | 18.0 ± 1.5 | 125.0 ± 10.2 | |
| Flexor carpi radialis 2† | OCF | 54.0 ± 0.8 | 75.0 ± 0.9 | 21.0 ± 0.9 | 149.0 ± 8.1 |
| Sham | 54.0 ± 0.8 | 76.0 ± 0.9 | 21.0 ± 0.9 | 147.0 ± 8.1 | |
| Flexor carpi ulnaris | OCF | 93.0 ± 0.9 | 34.0 ± 1.2 | 42.0 ± 1.5 | 288.0 ± 10.4 |
| Sham | 93.0 ± 0.9 | 33.0 ± 1.2 | 40.0 ± 1.5 | 277.0 ± 10.4 | |
| Long head of the triceps brachii | OCF | 82.0 ± 6.2 | 18.0 ± 6.3 | 37.0 ± 1.5 | 254.0 ± 11.1 |
| Sham | 80.0 ± 6.2 | 16.0 ± 6.2 | 36.0 ± 1.5 | 247.0 ± 11.0 | |
| SDF | OCF | 90.0 ± 2.2 | 34.0 ± 1.6 | 41.0 ± 1.6 | 280.0 ± 11.6 |
| Sham | 89.0 ± 2.3 | 33.0 ± 1.7 | 42.0 ± 1.7 | 285.0 ± 12.1 | |
| Humeral head of the DDF | OCF | 86.0 ± 1.4 | 36.0 ± 1.3 | 45.0 ± 1.7 | 306.0 ± 17.9 |
| Sham | 91.0 ± 1.4* | 35.0 ± 1.3 | 45.0 ± 1.7 | 334.0 ± 17.7 |
Stride duration was normalized to 100%, with the stance duration representing 0% to 48% of the stride and swing duration representing 49% to 100% of the stride.
Within a muscle within a variable, value differs significantly (P ≤ 0.05) from the value for the OCF limb.
Flexor carpi radialis 1 and 2 represent the first and second period of muscle activation during a single stride, respectively.
Onset of EMG activity for the ulnaris lateralis muscle began immediately before ground contact (90% of stride duration) and continued through most of the stance phase (35% of stride duration; Table 2). Onset of muscle activity was significantly (P = 0.05) delayed within the OCF limb, compared with results for the sham-operated limb (Figure 2). Onset of muscle activity for the ulnaris lateralis muscle was also significantly (P = 0.02) affected by creation of an OCF and the type of exercise treatment. Within the control group, the OCF limb had a significantly (P = 0.004) delayed onset of activity for the ulnaris lateralis muscle activity (91 ± 1% of stride duration), compared with that for the ulnaris lateralis muscle in the sham-operated contralateral limb (88 ± 1%). However, there were no significant differences between the OCF and sham-operated limbs within the UWT exercise group.
Graph of a representative processed EMG activation profile for the ulnaris lateralis muscle of OCF (black line) and sham-operated (gray line) limbs. The onset (arrows) and termination (arrowheads) of muscle activity for the OCF (black symbols) and sham-operated (gray symbols) limbs differed significantly (P ≤ 0.05).
Citation: American Journal of Veterinary Research 78, 5; 10.2460/ajvr.78.5.558
The EMG activity of the humeral head of the DDF muscle began immediately before ground contact (86% of stride duration), and the muscle remained active through most of the stance phase (35% of stride duration). Creation of an OCF significantly (P = 0.02) affected timing of DDF muscle activation and duration of activity. The presence of an OCF caused the DDF muscle to activate earlier, remain active for a longer period, and deactivate later in the stride, compared with results for the sham-operated limb (Table 3). Horses exercised in the UWT had significantly (P = 0.01) shorter durations of activation for the DDF muscle and earlier periods of deactivation in the OCF limb, compared with results for the OCF limb of the control group.
Clinical examination
Several factors were evaluated during clinical examinations.
Lameness—A persistent mild degree of lameness (mean ± SEM, 1.81 ± 0.05) was evident within all OCF limbs, which differed significantly (P < 0.001) from baseline values (0.03 ± 0.09). Lameness scores within the OCF limbs for the UWT exercise group were significantly (P = 0.04) higher at day 21 (7 days after the initiation of UWT exercise; 2.5 ± 0.2), compared with lameness scores for the OCF limbs of the control group at day 21 (2.0 ± 0.2). At days 42 and 49 (28 and 35 days after initiation of UWT exercise, respectively), lameness scores for the OCF limbs of the UWT group were significantly (P = 0.04) lower, compared with lameness scores for the OCF limbs of the control group.
Carpal joint flexion—Mean ± SEM scores for the response to carpal joint flexion were significantly (P < 0.001) higher for OCF (1.8 ± 0.1) than for sham-operated (0.1 ± 0.1) joints in all horses; this pattern persisted throughout the study. A significant (P = 0.01) treatment effect was found for flexion scores because OCF joints of the UWT group were significantly more responsive (1.9 ± 0.1) than were OCF joints of the control group (1.6 ± 0.1). Least squares mean comparisons of OCF joints for the UWT group over the entire study period revealed that there were significantly higher limb flexion responses on days 35, 56, and 63.
Radiography—A significant increase in radiographically detected middle carpal joint lesions was evident for all radiographic outcome variables after creation of an OCF. There was no significant difference in radiographic scores between the UWT and control groups at baseline or day 14. Analysis of subjective radiographic scores at day 70 indicated that UWT exercise caused an increase in lytic changes within the radial carpal bone. At study conclusion (day 70), OCF joints of the UWT group had a significantly (P < 0.001) higher score for subchondral bone lysis (2.6 ± 0.2), compared with the score for the OCF joints of the control group (1.6 ± 0.2). Cumulative radiographic scores for sham-operated (0.2 ± 0.3) and OCF (3.4 ± 0.3) joints were significantly different (P < 0.001) at day 14 (prior to treatment). Cumulative radiographic scores were significantly higher (P = 0.001) for OCF joints of the UWT group (7.4 ± 0.4), compared with scores for OCF joints of the control group (5.3 ± 0.4) at day 70.
Goniometry—Creation of an OCF resulted in significantly (P = 0.01) lower carpal flexion angles throughout the study period. Presence of an OCF in association with joint pain and inflammation reduced the carpal joint passive range of motion. Mean ± SEM flexion angle of the carpal joint of OCF limbs (33.0 ± 0.8°) was significantly larger than that of sham-operated limbs (25.0 ± 0.8°). Flexion angle of the carpal joint of OCF limbs was also significantly (P = 0.02) different for the UWT group (31.0 ± 1.0°), compared with results for OCF limbs of the control group (34.0 ± 1.0°). Exercise in a UWT improved carpal joint passive range of motion. Significant improvements in carpal joint flexion angles within the UWT group began on day 21 and continued throughout the remainder of the study. At study conclusion, there was no significant difference in passive range of motion of the carpal joint between the OCF and sham-operated limbs of the UWT group; exercise in a UWT returned carpal joint range of motion to baseline values.
Shoulder joint extension and elbow joint flexion were both significantly affected by creation of an OCF. Shoulder joint extension was significantly (P = 0.01) greater in the OCF limbs (134.0 ± 0.9°) than in the sham-operated limbs (133.0 ± 0.9°). Elbow joint flexion (62.0 ± 0.9°) was significantly (P = 0.002) different in the OCF limbs than in the sham-operated limbs (60.0 ± 0.9°). There were no significant effects of treatment on flexion and extension of the shoulder joint, elbow joint, or metacarpophalangeal joint.
Histologic examination
Evaluation of sections of articular cartilage stained with safranin O-fast green stain revealed no substantial loss of stain deposition in any of the 4 evaluated regions within the OCF or sham-operated joints or between treatment groups. Histologic evaluation of articular cartilage sections stained with H&E stain revealed that within the third carpal bone, OCF joints had significantly (P = 0.02) higher numbers of chondrone formations (1.7 ± 0.2), compared with numbers for the sham-operated joints (1.0 ± 0.0). Further morphological analysis for articular cartilage fibrillation, focal cell loss, and chondrocyte necrosis by use of H&E stain revealed no significant differences on the basis of induction of osteoarthritis at any of the 3 carpal bone locations. Exercise in a UWT did not significantly affect articular cartilage histologic morphology.
Creation of an OCF and exercise in a UWT did not result in significant changes in synovial membrane vascularity, subintimal fibrosis, or cellular infiltration. However, significantly (P = 0.009) more synovial membrane intimal hyperplasia was detected within the OCF joints (mean ± SEM score, 1.5 ± 0.2), compared with the score for the contralateral sham-operated joints (0.6 ± 0.2). In addition, a significant (P = 0.05) treatment effect was evident, with less intimal hyperplasia in sham-operated joints of the UWT group (0.1 ± 0.3), compared with scores for the sham-operated joints of the control group (1.1 ± 0.3). Exercise in a UWT helped to reduce the inflammatory response associated with synovitis.
Discussion
To our knowledge, the randomized controlled study reported here was the first in which clinical and biomechanical effects of UWT exercise on measures of musculoskeletal function and the development and progression of osteoarthritis have been evaluated. Quantification of muscle activation patterns in conjunction with thoracic limb kinetics and kinematics provided novel insights into the adaptive and maladaptive compensatory mechanisms associated with joint pain and osteoarthritis. The present study provided evidence that aquatic treatment for the management of carpal joint osteoarthritis has synovial membrane anti-inflammatory effects and can result in measurable clinical improvements. Exercise in a UWT was able to reestablish baseline values for passive flexion of the carpal joint, which resulted in returning the carpal joint to a full passive range of motion. In addition, horses exercising in the UWT had evenly distributed thoracic limb axial loading and symmetric timing of selected thoracic limb musculature. The improvement in clinical signs of osteoarthritis in horses of the UWT exercise group was further supported by evidence of decreased inflammation during histologic examination. Exercise in a UWT significantly decreased the degree of inflammatory infiltrate in the synovial membrane.
Radiographic evidence of lysis within the radial carpal bone is routinely detected after use of the OCF technique.30 The increase in lysis seen in the horses exercising in a UWT in the present study was believed to be the combined result of the aquatic exercise and technique because when the OCF was surgically created, it initially was displaced from the parent bone but remained attached to the proximal aspect of the joint capsule. The increase in carpal joint range of motion appreciated during UWT exercise and the increase in resistance in sagittal plane motion at the higher levels of water may have increased tensile stresses on the joint capsule and caused micromotion of the OCF. Although radiography can be valuable in characterizing structural changes within osteoarthritis-affected joints, it was unable to differentiate adaptive from pathological changes attributable to UWT exercise.
Passive range of motion exercises have been advocated for human patients after arthroscopic surgery to aid in preventing joint capsule fibrosis and improve healing of articular cartilage defects.31–33 The primary goals of passive joint range of motion exercise are to prevent periarticular tissue fibrosis, maintain tissue mobility, improve vascular dynamics, allow for synovial fluid diffusion, and decrease pain.31–34 Similarly, aquatic treatments for horses may be used to improve joint health via low-impact controlled exercise. Early use of aquatic treatments may help reduce edema, improve joint range of motion, minimize joint capsule fibrosis, and enhance fluid exchange within injured joints.9,35 Horses in both treatment groups of the present study had the largest decrease in passive carpal joint flexion during the first week after surgery. Horses exercising in a UWT began to increase passive carpal joint flexion within OCF joints by 1 week after the initiation of aquatic treatment, and this increase continued to the end of the study whereby passive carpal joint flexion was restored to baseline values.
The clinical lameness response to carpal joint flexion within OCF joints in the UWT exercise and control groups was negligible. Although there was a significant difference for the response of the OCF limb of the UWT exercise group (1.95 ± 0.08) and the control group (1.66 ± 0.08), the difference was too small to be of practical value. In addition, subtle lameness and the response to flexion is difficult to detect, and lameness examinations performed by both experienced and inexperienced veterinarians is subjective, with high interobserver and intraobserver variability.36,37 The validity of conducting flexion tests during lameness evaluations has been questioned because false-positive results are more common in nonlame working horses.38,39 Thus, the difference in the response to carpal joint flexion during the lameness examination was determined to be a small value that had no meaningful impact and thus was clinically irrelevant.
Equine biomechanical studies40–45 have documented the presence of compensatory gait patterns associated with various types or severity of musculoskeletal lameness. Typically, a horse will modify its gait to reduce loading of a lame limb and compensate by redistributing weight bearing to the other limbs. In an effort to sustain the impulse needed for propulsion, stance duration of the lame limb will increase while achieving a lower peak vertical force.40 Mild lameness often causes a decreased peak vertical GRF within the lame limb, whereas compensatory changes in the remaining limbs are not observed.40 Induction of subtle lameness by use of a transient method of sole pressure results in significant changes in peak vertical force and stance duration only within the lame thoracic limb,41 whereas induction of a moderate degree of lameness also influences GRF parameters in the contralateral thoracic and bilateral pelvic limbs.40,41 Results for a method for unilateral induction of synovitis by use of amphotericin B in 1 carpal joint indicate that stance phase measurements are not significantly influenced by induction of a moderate degree of lameness (scores ranging from 2.5 to 3.0 ± 0.3).46 Conversely, creating a 1-cm-diameter, full-thickness articular cartilage defect on the dorsolateral aspect of the distal radial carpal bone results in an easily observable lameness and significant alterations in both vertical and craniocaudal GRF components.47 Therefore, the reliability of force platform analysis to detect compensatory load redistribution patterns appears to be partially influenced by the severity of the experimentally induced lameness.
In the present study, a treatment effect was detected because horses in the UWT exercise group had symmetric limb loading and had similar peak vertical forces and vertical loading rates in the OCF and sham-operated thoracic limbs. The OCF limbs within the control group had a significantly lower loading rate, lower amount of weight bearing, and prolonged stance duration, which was indicative of a protective mechanism adopted to reduce mechanical stresses. Prolonged stance duration reflects a compensatory mechanism used to distribute weight-bearing forces over a longer duration, thus reducing the magnitude of vertical GRFs.41
Kinematic analyses of horses with naturally occurring and experimentally induced carpal joint osteoarthritis revealed that these horses often have asymmetries during the swing phase of the gait, with fewer alterations detected during the stance phase.43,46,48 Creation of an OCF in the middle carpal joint in the study reported here resulted in an overall reduction in swing phase peak flexion angles of the shoulder, elbow, and carpal joints, which is a characteristic of an extended limb and circumducting gait pattern used to minimize pain attributable to carpal joint flexion typically appreciated during lameness evaluation isolated to the carpal joints.49 During the stance phase, the proximal joints within the OCF limb also had greater extension angles, whereas the sham-operated limb had greater flexion angles at the shoulder and elbow joints. Experimentally induced lesions within the SDF tendons also cause increased extension of the shoulder and elbow joints of the affected limb during the stance phase.50 The extended position of the proximal articulations of the thoracic limb may be a compensatory mechanism adopted to stabilize limb function. The OCF method resulted in mechanical alterations that caused both a supporting and swinging limb lameness.
Results of EMG indicated significant changes in the OCF limb for muscles responsible for stabilization of the carpus (ie, ulnaris lateralis muscle) and subtle changes within the DDF muscle. The presence of acute joint pain and inflammation resulted in possible dysfunction and weakness of the ulnaris lateralis muscle. Assessment of the timing for the ulnaris lateralis muscle indicated that horses in the UWT exercise group maintained symmetric muscle activation, whereas the control group had delayed onset of muscle activation. Similar to results for the ulnaris lateralis muscle, creation of an OCF in the middle carpal joint induced alterations in DDF muscle activity that resulted in prolonged duration of activation and earlier onset of activation adopted to aid in carpal joint flexion and stabilization during the stance phase. However, the use of aquatic treatment resulted in shorter durations of DDF muscle activation and earlier periods of deactivation; thus, UWT exercise was able to establish the need for less motor recruitment of the DDF muscle during the stance and swing phases of a stride.
Neuromotor control of on-off muscle timing is crucial for producing coordinated movements and maintaining joint stability. Induction of osteoarthritis in the middle carpal joint of the present study caused asynchronous muscle activation patterns, which ultimately may have influenced the magnitude and rate of limb loading, impaired proprioception, and altered active joint range of motion. These neuromuscular alterations may have been the result of joint pain and inflammation, which altered afferent signals from joint mechanoreceptors and thus influenced the ability to coordinate muscle activity. Use of aquatic treatment resulted in an ability to maintain symmetric timing of select carpal musculature. Exercising in a UWT maintained timely neuromotor control between the thoracic limbs, which contributed to coordinated muscle activity, symmetric limb loading, and functional joint stability. Conversely, the delayed muscle activation within the OCF limbs of the control group may have contributed to an imbalance in muscle timing that led to incoordination and unequal attenuation of mechanical stresses applied across the middle carpal joint. Additional studies are needed to determine whether the ability of UWT exercise to reestablish or maintain neuromotor control is critical for optimizing performance and overall athletic function.
Clinical application of EMG evaluations has been limited because of the inherent variability for the obtained results. An EMG analysis commonly reveals large intraindividual and interindividual variation, even among individuals performing the same task.51 Variability in surface EMG recordings are often a result of movement of the skin, changes in skin impedance (conductivity of skin), differences in thickness and electrical properties of the tissue layers between the surface electrodes and muscles, location of electrodes, cross talk (interference in the EMG signal attributable to electrical activity of surrounding musculature), and morphometric variability in muscle mass and fiber type. The vast degree of variability is not surprising because the volume of muscle is large relative to the region sampled by the surface electrodes. Surface EMG electrodes only record activity from the superficial portion of a muscle belly, such that the EMG signal recording is sensitive to compartmentalization of recruitment patterns within the muscle.52 Intrinsic muscles of the thoracic limbs reportedly have anatomic subregions that differ in fiber type and orientation.53,54 These anatomic subregions function independently, which results in an inability to characterize activity of an entire muscle within the limited recording volume of the EMG electrodes.55 Investigators may want to evaluate changes in muscle activity within a muscle's anatomic subregions by use of a combination of surface and fine-wire EMG electrodes. The large variability for the EMG signal recorded by use of the fine-wire electrodes may have been attributable to the inability to sample from the same motor units at each data collection time point. Wire migration, cable motion artifact, and weak electrical connection between the wires and spring cables also may have contributed to a greater degree of variation in the EMG signal. Although the inherent variability associated with EMG data collection and the intrinsic anatomic differences within muscles compound the difficulty for assessment of EMG changes over time, it is essential that investigators address the issue of differentiating normal and pathological neuromuscular changes associated with joint pathological processes. A better understanding of these defense mechanisms would be expected to provide equine practitioners with improved treatment and rehabilitation protocols that are focused on treating the primary injury but also on preventing the development of osteoarthritis and other compensatory musculoskeletal injuries.
An additional constraint for the present study was the inability to capture out-of-plane motion. Analysis of the kinematic data revealed that most of the significant differences occurred during the swing phase; thus, out-of-plane motion may have further influenced the gait with a potential for a treatment effect. However, only sagittal plane motion could be determined by use of the optical capture system used in the study reported here. In addition, subtle clinical signs associated with OCF and the short duration of the study may have limited the comparison of biomechanical alterations in the thoracic limbs over time.
The purpose of the study reported here was to evaluate whether UWT exercise can be an effective treatment procedure to decrease the consequences of experimentally induced carpal joint osteoarthritis and to establish validated treatment protocols that minimize maladaptive compensatory mechanisms attributable to joint pain and inflammation. The increase in lameness scores for the aquatic treatment group 1 week after initiation of UWT exercises was believed to be a result of the OCF technique. Typically, OCFs would be removed from clinically affected animals during surgery; thus, the precise timing of UWT exercise still needs to be determined. Studies32,33 on various forms of range of motion exercises have revealed improvements in articular tissue healing when the exercises are started 1 week after surgery, compared with results when range of motion exercises are started 3 weeks after surgery. On the basis of conclusions from those studies,32,33 application of range of motion exercises should begin the first week after surgery to achieve superior tissue healing. It may be more appropriate for the initial management of osteoarthritis to exercise at a lower water level, which would promote an increase in joint flexion and extension ranges of motion without the initial resistance of water at higher levels. Water of various depths promotes joint-specific increases in ranges of motion, which therefore provides the ability to adapt treatment protocols to target certain joints. However, the increases in joint range of motion at lower water levels must be weighed against the importance of decreasing load-bearing stress across joint surfaces provided by the effects of buoyancy. Therefore, additional studies are needed to establish validated treatment protocols. Nevertheless, the study reported here provided a contribution to the equine industry because it was one of the first to provide evidence-based support for aquatic treatment of horses.
Acknowledgments
Supported by discretionary funds from the Colorado State University Orthopaedic Research Center.
The authors declare that there were no conflicts of interest.
ABBREVIATIONS
| CV | Coefficient of variation |
| DDF | Deep digital flexor |
| EMG | Electromyography |
| GRF | Ground reaction force |
| OCF | Osteochondral fragment |
| SDF | Superficial digital flexor |
| UWT | Underwater treadmill |
Footnotes
Equigym, Equigym LLC, Lexington, Ky.
Equine underwater treadmill, Ferno Veterinary Systems, Wilmington, Ohio.
MEK 92-PAD photoelectric control, Mekontrol Inc, Northboro, Mass.
Bertec force platforms, Model FP6090-15, Bertec Corp, Columbus, Ohio.
Super glue (cyanoacrylate adhesive), Pacer Technology, Rancho Cucamonga, Calif.
Motus software, version 9.1, Vicon, Centennial, Colo.
200 Hz cameras, Vicon, Centennial, Colo.
Dormosedan, Pfizer Inc, New York, NY.
Blue Sensor, Ambu Inc, Glen Burnie, Md.
Agri Labs, St Joseph, Mo.
Stainless steel 7-strand teflon-coated fine-wire electrode spool, A-M Systems Inc, Sequim, Wash.
3–0 Monocryl, Ethicon, San Angelo, Tex.
Noraxon Telemyo 2400 G2, Noraxon USA, Scottsdale, Ariz.
Extendable goniometer, Lafayette Instrument Co Inc, Lafayette, Ind.
GLIMMIX, SAS, version 9.3, SAS Institute Inc, Cary, NC.
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Appendix
Thoracic limb muscles instrumented with surface or fine-wire electrodes to record EMG activity and the approximate anatomic location for electrode placement.
| Thoracic limb musculature | Electrode | Location of electrode |
|---|---|---|
| Extensor carpi radialis | Surface | Cranial aspect of the radius at a point 8 cm distal to the olecranon |
| Ulnaris lateralis | Surface | Lateral aspect of the radius at a point 12 to 15 cm distal to the olecranon |
| Flexor carpi radialis | Surface | Medial aspect of the radius at a point 10 cm distal to the olecranon |
| Flexor carpi ulnaris | Surface | Medial aspect of the radius at a point 10 cm distal to the olecranon |
| Long head of the | Surface | On a horizontal line at a point 25 cm caudal to the triceps brachii tuberculum majus pars cranialis |
| SDF | Fine-wire | Palmar aspect of the radius at a point 9 to 12 cm proximal to the carpal accessory bone at a depth of 1.0 to 1.5 cm |
| Humeral head of the DDF | Fine -wire | Palmar aspect of the radius at a point 9 to 12 cm proximal to the carpal accessory bone at a depth of 2.0 to 2.5 cm |
