Osteoarthritis is a common cause of distal tarsal pain in horses,1 but there is limited information on the etiopathogenesis of this condition. Although degenerative lesions on all aspects of the joints have been reported, standard imaging has revealed these lesions are most commonly in the dorsomedial aspect of the CD joint and the dorsolateral aspect of the TMT joint.2 Whether these are true sites of predisposition in horses with early stages of pathological change and the reason for these apparent predisposition sites have not been investigated to our knowledge.
Overloading of the osteochondral tissues is considered a likely factor in osteoarthritis development, as is exercise-associated osteochondral damage.3 Elite show jumpers reportedly have a higher prevalence of distal tarsal osteoarthritis than horses undergoing general purpose exercise, which may reflect a response to overloading.4 However, there has been little evaluation of relationships between exercise type and tarsal osteoarthritis location and type.
At the level of the TMT joint, compressive strains are highest dorsally and laterally as suggested by strain-gauge evidence.5 This finding is also supported by nuclear scintigraphic evidence of radiopharmaceutical uptake patterns across the distal tarsal bones from horses with no history of hind limb lameness. The uptake pattern appears repeat-able between horses, and uptake is greatest dorsally and laterally, indicating an increase in bone remodelling and supporting these regions as high-load sites.6 It has been proposed that farther proximally, there is a transfer of load from proximal to distal in a medial to lateral direction from the tibia to the proximal metatarsal region.7
Hyaline cartilage, CC, and SCB thicknesses in horses are affected by exercise, age, and location within a joint.7–16,a,b Particular locations within a joint are likely to be most susceptible to osteochondral damage as a result of varying loading patterns across articular surfaces.7,8,17–19 Specifically in the distal tarsal joints, elite-level competition training is associated with an increase in SCB thickness and alters the mediolateral and proximodistal SCB thickness pattern.20 Thicker SCB can be found at the medial aspect of the CD joint and the lateral aspect of the TMT joint than in the other locations in those joints, supporting these as high-load sites. Thickness of the HC, CC, and SCB of the tarsal osteochondral unit appears to reflect the loading patterns across the articular surface for both the CD and TMT joints.21
Horses that are ridden have increased loading due to the weight of the rider and various loading patterns, depending on the level and type of work they are performing. Intense competition training involves a great reliance on power from the hindquarters, which increases the hind limb load and tarsal compression for a greater proportion of the stride,22 and jumping increases the loading on the dorsal aspect of the tarsus, with greater tarsal compression at takeoff.23
The purpose of the study reported here was to determine the presence and location of exercise-related histopathologic changes in the CD and TMT (distal tarsal) joints of horses with no history of hind limb lameness and to determine locations in equine distal tarsal joints that were predisposed to osteoarthritis, whether the osteoarthritis process was more advanced at these locations when the joints were subjected to increased loading, and whether the distribution of lesions would change with increased loading. The hypotheses were that low-intensity and high-intensity, elite competition horses would have more osteochondral lesions than would pasture-exercised horses and that at sites predisposed to osteoarthritis, there would be higher histopathologic scores than at sites not predisposed to osteoarthritis in each of the various exercise groups. Furthermore, we hypothesized that the depth and shape of the lesion would be correlated with the cellular arrangement within the cartilage, the organization of the HC-CC and CC-SCB junctions, and the organization of the SCB.
Materials and Methods
Sample population—Cadaver tarsal joints of 30 horses with no history or clinical evidence of hind limb lameness when examined by an experienced orthopedic clinician (SJD) and no radiographic evidence of abnormality were included in the study. These horses had been euthanatized for reasons other than the present study. Tarsi were collected within 6 hours after death and stored at −20°C.
Group allocation—Tarsi were allocated to 1 of 3 groups, depending on the exercise status of the originating horse. Group P consisted of 10 tarsi from 5 mature female Thoroughbred horses (mean age, 14 years; range, 10 to 19 years) that had raced at 2 years of age and had subsequently been restricted to only pasture exercise for a mean period of 13 years (range, 9 to 16 years). Group L consisted of 6 left and 4 right tarsi from 6 mature horses (mean age, 11 years; range, 7 to 15 years) that had a history of low-intensity, ridden exercise, defined as low-intensity exercise on mixed terrain and unaffiliated competition. Four of these horses were castrated males, and 2 were female; 2 were Thoroughbred crosses, and 4 were warmblood horses. Group E consisted of 5 left and 5 right tarsi from 6 mature horses (mean age, 12.9 years; range, 10 to 17 years) with a history of high-intensity, elite competition exercise. Elite competition was defined as high-level national or international show jumping, dressage, or 3-day eventing competition, which includes jumping, galloping, tight turns, and gymnastic-type exercises. All 6 horses were castrated males; 2 were Thoroughbred crosses, and 4 were warmblood horses.
Histologic preparation—To define medial (30% of the medial-lateral width of the third tarsal bone), midline (50%), and lateral (70%) sites on each tarsus for sectioning, sites previously defined on sagittal 3-D T1-weighted spoiled gradient echo magnetic resonance images were translated onto each frozen tarsus as described elsewhere.21 A large band sawc was used to cut the distal tarsal joints into sagittal slices 4 to 5 mm thick. Slices were detached by cutting in a transverse plane above the talocalcaneal-centroquartal (proximal intertarsal) joint. The chosen medial, midline, and lateral slices were cut in a transverse and then a dorsal plane to produce dorsal sections through the distal tarsal joints that were half the dorsal-to-plantar depth of the third tarsal bone.
Initially, samples were fixed in neutral-buffered 10% formalin for 10 days and then placed in rapid decalcifierd for 2 days. Following decalcification, the sections were washed under running water for 1 day prior to serial dehydration in 70%, 90%, and 3 changes of 100% alcohol, then 3 changes of xylene and 3 changes of molten histologic waxe on an automatic tissue processor.f The sections were finally embedded in blocks of paraffin wax.
Sections were cut at 6 μm, mounted on gelatin-coated slides, and dried in an oven at 37°C. Two slides were prepared per section; 1 slide was stained with Harris H&E, and the other was stained with 1% toluidine blue. The stained sections were then mounted in mountant.g
Histopathologic scoring—Morphological characteristics of cartilage and SCB in histologic preparations were determined by microscopic examination.h A grading system was adapted from 2 previous studies22,23 in which other animal species were evaluated (Appendix). The location, depth, and shape of each lesion; the cellular arrangement within the cartilage; the organization of the HC-CC and CC-SCB junctions; and the organization of the SCB were assessed. A high score signified more severe pathological change than a low score. A single lesion was defined as a lesion located on 1 aspect of the joint, and an adjoining lesion was defined as a lesion located on both adjacent aspects of a joint. A collapsed junction was said to exist when the HC-CC or CC-SCB junction was not clearly visible or when there was considerable indentation. Scores were assigned for the distal aspect of the central tarsal bone, proximal and distal aspects of the third tarsal bone, and proximal aspect of the third metatarsal bone. The 4 articular surfaces were divided into 4 areas (Figure 1), and a score was assigned to each area at the medial, midline, and lateral sites, which were 30%, 50%, and 70% of the medial-lateral width of the third tarsal bone, respectively (Figure 2). Interobserver repeatability between an experienced equine histopathologist (ASB) and a second trained observer (CAT) was assessed at each site by use of 10 repeated scorings/site for 10 limbs. Final scores were obtained when the coefficient of variation was < 2%. The second trained observer carried out all histologic interpretations.
Diagram of the sagittal view of an equine tarsus. The CD joint forms the articulation between the central tarsal bone (CT) and the third tarsal bone (T3). The TMT joint forms the articulation between the T3 and the third metatarsal bone (MT3). Notice areas A, B, C, and D from which specimens were obtained for histologic evaluation.
Citation: American Journal of Veterinary Research 72, 1; 10.2460/ajvr.72.1.33
Diagram of a dorsal view of an equine tarsus. Notice the medial, midline, and lateral sites (lines at 30%, 50%, and 70% of the width of the T3, respectively, measured from the medial aspect) from which specimens were obtained for histologic evaluation. There were 4 sites from each bone for histologic evaluation. See Figure 1 for key.
Citation: American Journal of Veterinary Research 72, 1; 10.2460/ajvr.72.1.33
Statistical analysis—Descriptive statistics were calculated to describe the histologic characteristics of various regions of the articular surface within each exercise group. Spearman rank correlation coefficients (ρ) were calculated to investigate relationships among groups with respect to histopathologic characteristics. Strengths of correlations were defined as follows: weak, 0.20 to 0.39; modest, 0.40 to 0.69; strong, 0.70 to 0.89; and very strong, > 0.90.24
Statistical tests were carried out by use of only 1 limb/horse and 2 limbs/horse to test for pseudoreplication. All analyses were performed with statistical analysis software.i Significance was defined as a value of P < 0.05.
Results
Histopathologic description of cartilage and SCB at sites with no lesions—In group P (pasture exercise only), the cellular arrangement was characterized by evenly spaced cells of uniform density. The matrix was evenly stained throughout each section. Small numbers of chondrocyte clusters and chondrones were seen in the superficial layer of the HC. In all sections, the HC-CC and CC-SCB junctions were clearly defined, with small clusters of cells merging into the junction. Multiple arrest lines were visible in the CC. The SCB had a uniform appearance with no enlarged bone spaces; however, there was evidence of intense secondary bone remodeling (Figure 3).
Photomicrograph of a tissue section obtained from the medial aspect of the CD joint of a 12-year-old Thoroughbred female from group P (pasture exercise only). Notice the chondrones in the superficial layer of the HC (black arrows). There are secondary SCB remodeling and some remnants of calcified cartilage extending into the SCB (gray arrows). CT = Central tarsal bone. Toluidine blue stain; bar = 200 μm.
Citation: American Journal of Veterinary Research 72, 1; 10.2460/ajvr.72.1.33
As in group P, the cellular arrangements in groups L (low-intensity exercise) and E (high-intensity, elite competition exercise) were characterized by evenly spaced cells of uniform density. Small numbers of chondrocyte clusters and chondrones were scattered throughout the HC and CC layers. Cellular arrangements at the HC-CC and CC-SCB junctions were clearly defined with small clusters of cells merging into them. In 2 limbs, the junctions were not as clearly defined with an appearance of junction collapse. The SCB had a uniform appearance, but bone spaces were slightly enlarged relative to the sizes of the bone spaces in group P (Figure 4).
Photomicrograph of a tissue section obtained from the medial aspect of the distal articular surface of the central tarsal bone (CT) of an 8-year-old castrated male Thoroughbred-Irish Draught cross from group L (low-intensity, ridden exercise). The SCB spaces (asterisks) are enlarged, compared with those in Figure 3. Toluidine blue stain; bar = 200 μm.
Citation: American Journal of Veterinary Research 72, 1; 10.2460/ajvr.72.1.33
Histopathologic changes in cartilage and SCB—All pathological changes seen in all 3 exercise groups were at the dorsal aspect of the CD and TMT joints. Of all 10 limbs in group P, 3 joints from 3 horses had lesions. One lesion was on the distal lateral aspect of the central tarsal bone in 1 joint and the proximal lateral aspect of the third metatarsal bone in another joint. An adjoining lesion was at the midline site of the TMT joint (Figure 5). Large numbers of chondrones were present in the HC surrounding the adjoining lesion, and at the proximal lateral aspect of the third metatarsal bone, there was focal total cellular loss. At all 3 sites with lesions, the HC-CC and CC-SCB junctions were totally collapsed. The SCB spaces in those 3 sites were also enlarged relative to sites with no lesions.
Photomicrograph of a tissue section obtained from the midline aspect of the TMT joint of a 12-year-old Thoroughbred female from group P (elite competition exercise). Notice the mild hillock and cavitation formation, with chondrones present in the HC (black arrow). There is loss of the CC layer and CC-HC junction (green arrow). Toluidine blue stain; bar = 200 μm. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 72, 1; 10.2460/ajvr.72.1.33
In group L, 50% of the joints had osteochondral lesions. There were 4 adjoining lesions at the medial site of the CD joint and 2 at the midline site of the CD joint. Three adjoining lesions were detected in the same TMT joint: 1 medial, 1 midline, and 1 lateral. All adjoining lesions were more severe than the one in group P (Figure 6). Fragmentation of the cartilage layer with total focal loss and disruption of the CC layer was also apparent at the midline site of the CD joint. In addition, there was loss of the typical cellularity in the HC layer focally around the defect with a large number of chondrones present in the HC and CC (Figure 7). As well as the cartilage fragmentation, an SCB lesion was evident on the distal aspect of CT, which was associated with the cartilage lesion. New bone formation was detected in the area directly below the CC layer (Figure 8). In the lateral aspect of the TMT joint, 2 adjoining V-shaped lesions were detected (Figure 9). The area surrounding the defects had large chondrones within it. The HC-CC and CC-SCB junctions were less clearly defined with chondrocyte clusters merging into them. The organization of the SCB was similar to that of group P; however, the bone spaces were slightly enlarged in comparison.
Photomicrograph of a tissue section obtained from the medial aspect of the CD joint of an 8-year-old castrated male warmblood horse from group L. The hillock and cavitation (asterisks) are more pronounced than those seen in Figure 5. There are a large number of chondrones in the HC (black arrow). Collapse of the CC-HC junction (green arrow) and enlarged SCB spaces are evident. Toluidine blue stain; bar = 200 μm. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 72, 1; 10.2460/ajvr.72.1.33
Photomicrograph of a tissue section obtained from the midline aspect of the CD joint from an 8-year-old castrated male warmblood horse from group L. Total cellular loss is visible, and there are large chondrones (arrows) on both sides of the joint, surrounding the full-thickness AC defect. Toluidine blue stain; bar = 200 μm. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 72, 1; 10.2460/ajvr.72.1.33
Photomicrograph of a tissue section obtained from the lateral aspect of the TMT joint of a 15-year-old female warmblood horse from group L (low-intensity, ridden exercise). Notice the dip on the articular surface of the third metatarsal bone (MT3; asterisk). New bone formation was detected on the distal aspect of the third tarsal bone (T3; arrow). Toluidine blue stain; bar = 200 μm.
Citation: American Journal of Veterinary Research 72, 1; 10.2460/ajvr.72.1.33
Photomicrograph of a tissue section obtained from the medial aspect of the CD joint of a 12-year-old castrated male warm-blood horse from group E (high-intensity, elite competition exercise). Notice how similar this image is to Figure 5, with the mild hillock and cavitation formation. Total loss of the calcified cartilage layer is also evident on the distal aspect of the CT (arrow). Toluidine blue stain; bar = 200 μm. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 72, 1; 10.2460/ajvr.72.1.33
In group E, 1 adjoining lesion was detected in the CD joint and 3 were detected in the TMT joint; the 4 lesions observed in group E were seen in 4 separate joints. Two lesions on 1 side of the joint were also detected in the CD and TMT joints. These 6 lesions were distributed among 5 limbs (Table 1). At the medial aspect of the CD joint, an adjoining cavitation and hillock-type lesion appeared more severe than either of those in groups P and L. At the midline site of the CD joint, an adjoining fibrillation lesion was recorded. In the TMT joint at all 3 sites, adjoining cavitation and hillock formation appeared more severe than those in group P. A V-shaped lesion was evident at the lateral aspect of the same TMT joint. At all locations in which no lesions were detected, there was focal total cellular loss and total loss of the CC layer, but in the areas surrounding the lesions, large numbers of chondrones were seen. The HC-CC junction had collapsed at sites in which the CC layer was lost. The CC-SCB junction was also clearly defined with a large number of cellular clusters merging with it. In the lesion-free sites, the organization of the SCB was similar to that of groups P and L.
Total numbers of lesions detected on all 4 articular surfaces (proximal and distal CD joint and proximal and distal TMT joint) in cadaveric tarsi from nonlame horses that had a history of pasture exercise only (group P; n = 10), low-intensity exercise (group L; 10), or high-intensity, elite competition exercise (group E; 10).
| Group P | Group L | Group E | |||||||
|---|---|---|---|---|---|---|---|---|---|
| Articular surface | Med | Mid | Lat | Med | Mid | Lat | Med | Mid | Lat |
| Distal aspect of the CT | 0 | 0 | 0 | 3 | 2 | 0 | 1 | 2 | 0 |
| Proximal aspect of the T3 | 0 | 0 | 0 | 3 | 2 | 0 | 1 | 1 | 0 |
| Distal aspect of the T3 | 0 | 1 | 0 | 0 | 1 | 1 | 1 | 1 | 2 |
| Proximal aspect of the MT3 | 0 | 1 | 1 | 0 | 1 | 1 | 1 | 1 | 1 |
CT = Central tarsal bone. Lat = Lateral aspect. Med = Medial aspect. Mid = Mid aspect. MT3 = Third metatarsal bone. T3 = Third tarsal bone.
Histopathologic grading—The mode and median for scores of cellular arrangement on the distal aspect of the CT were higher on the medial side than on the lateral side in groups P and L. However, such values were consistent over the whole surface in group E. The mode and median for scores of organization of the junctions were consistent over the whole surface in all 3 exercise groups. The organization of SCB in group P had a higher score medially, whereas in groups L and E, the score was consistent over the whole articular surface (Table 2).
Modes of histopathologic scores for the appearance of the distal articular surface of the central tarsal bone in cadaveric tarsi from nonlame horses that had a history of pasture exercise only (group P; n = 10), low-intensity exercise (group L; 10), or high-intensity, elite competition exercise (group E; 10).
| Group P | Group L | Group E | |||||||
|---|---|---|---|---|---|---|---|---|---|
| Characteristic | Med | Mid | Lat | Med | Mid | Lat | Med | Mid | Lat |
| Cellular arrangement | 3 | 3 | 2 | 3 | 2 | 2 | 2 | 2 | 2 |
| Organization of cartilage junctions | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
| SCB organization | 2 | 1 | 1 | 0 | 0 | 0 | 1 | 1 | 1 |
Scores represent increasing degree of abnormality (see Appendix), with 0 indicating no abnormalities and 5 indicating severe abnormalities. See Table 1 for remainder of key.
In the proximal aspect of the third tarsal bone, the cellular arrangement score was higher medially versus laterally in groups P and L; the score was the same over the whole surface in group E. The organization of the junctions was similar to that for the distal aspect of the CT in all 3 exercise groups. The mode and median of histologic scores for SCB organization were highest medially and at the midline in group P and at the midline in groups L and E, relative to other regions (Table 3). In the distal aspect of the same bone, the cellular arrangement and organization of the junctions were consistent over the whole surface in all 3 exercise groups; the mode and median of histologic scores for SCB organization were higher at the medial and lateral sites in group P and at the medial and midline sites in groups L and E (Table 4).
Modes of histopathologic scores for the appearance of the articular surface of the proximal aspect of the third tarsal bone in cadaveric tarsi from nonlame horses that had a history of pasture exercise only (group P; n = 10), low-intensity exercise (group L; 10), or high-intensity, elite competition exercise (group E; 10).
| Group P | Group L | Group E | |||||||
|---|---|---|---|---|---|---|---|---|---|
| Characteristic | Med | Mid | Lat | Med | Mid | Lat | Med | Mid | Lat |
| Cellular arrangement | 3 | 3 | 2 | 3 | 3 | 2 | 2 | 2 | 2 |
| Organization of cartilage junctions | 1 | 1 | 1 | 2 | 1 | 1 | 1 | 1 | 1 |
| SCB organization | 1 | 1 | 0 | 0 | 1 | 0 | 0 | 2 | 1 |
See Tables 1 and 2 for key.
Modes of histopathologic scores for the appearance of the articular surface of the distal aspect of the third tarsal bone in cadaveric tarsi from nonlame horses that had a history of pasture exercise only (group P; n = 10), low-intensity exercise (group L; 10), or high-intensity, elite competition exercise (group E; 10).
| Group P | Group L | Group E | |||||||
|---|---|---|---|---|---|---|---|---|---|
| Characteristic | Med | Mid | Lat | Med | Mid | Lat | Med | Mid | Lat |
| Cellular arrangement | 2 | 2 | 2 | 2 | 2 | 2 | 3 | 2 | 2 |
| Organization of cartilage junctions | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
| SCB organization | 1 | 0 | 1 | 1 | 1 | 0 | 2 | 2 | 1 |
See Tables 1 and 2 for key.
Results for the cellular arrangement and organization of the junctions were the same for the proximal aspect of the third metatarsal bone as for the distal aspect of the third tarsal bone; however, the SCB organization differed. The higher scores were assigned at the mid-line and lateral sites in group P and at the lateral site in group L, whereas the score was the same over the whole surface in group E (Table 5).
Modes of histopathologic scores for the appearance of the articular surface of the distal and proximal aspects of the third metatarsal bone in cadaveric tarsi from nonlame horses that had a history of pasture exercise only (group P; n = 10), low-intensity exercise (group L; 10), or high-intensity, elite competition exercise (group E; 10).
| Group P | Group L | Group E | |||||||
|---|---|---|---|---|---|---|---|---|---|
| Characteristic | Med | Mid | Lat | Med | Mid | Lat | Med | Mid | Lat |
| Cellular arrangement | 2 | 2 | 3 | 2 | 2 | 2 | 2 | 2 | 2 |
| Organization of cartilage junctions | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
| SCB organization | 0 | 1 | 1 | 0 | 0 | 1 | 1 | 1 | 1 |
See Tables 1 and 2 for key.
Statistical analysis—Correlation coefficients calculated for 1 limb/horse were the same as those obtained when both limbs from the same horse were used. Therefore, results from both limbs are reported (Table 6). In group P, depth and shape of a lesion were significantly correlated with the cellular arrangement (weak correlation), organization of the HC-CC and CC-SCB junctions (modest correlation), and organization of the SCB (weak correlation). The cellular arrangement was also significantly correlated with the organization of the SCB (weak correlation). In group L, depth and shape of a lesion were significantly correlated with the cellular arrangement (modest correlation), organization of the HC-CC and CC-SCB junctions (modest correlation), and organization of the SCB (weak correlation). The cellular arrangement was also significantly associated with the organization of the SCB (modest correlation). In group E, depth and shape of a lesion were significantly associated with the organization of the HC-CC and CC-SCB junctions (weak correlation). However, cellular arrangement was moderately correlated with organization of the SCB. Strength of association between cartilage cellular arrangement and SCB organization appeared to increase with increasing exercise level; however, this was not verified statistically.
Spearman rank correlations (ρ) between histologic scores for the appearance of lesions in cadaveric tarsi from nonlame horses that had a history of pasture exercise only (group P; n = 10), low-intensity exercise (group L; 10), or high-intensity, elite competition exercise (group E; 10).
| Group P | Group L | Group E | ||||
|---|---|---|---|---|---|---|
| Characteristics | ρ | P value | ρ | P value | ρ | P value |
| Depth and shape of lesion vs cellular arrangement | 0.17 | 0.005 | 0.44 | <0.001 | 0.11 | 0.071 |
| Depth and shape of lesion at the HC-CC vs CC-SCB junctions | 0.67 | < 0.001 | 0.60 | <0.001 | 0.20 | 0.002 |
| Depth and shape of lesion vs SCB organization | 0.18 | 0.002 | 0.31 | <0.001 | 0.10 | 0.128 |
| Cellular arrangement vs SCB organization | 0.32 | < 0.001 | 0.45 | <0.001 | 0.55 | < 0.001 |
Strengths of correlations were defined as follows: weak, 0.20 to 0.39; modest, 0.40 to 0.69; strong, 0.70 to 0.89; and very strong, > 0.90.26 A value of P < 0.05 was used to indicate a significant correlation.
Discussion
Results of the study reported here supported the hypothesis that more osteochondral lesions would be present in low-intensity and elite-level competition- training horses than in pasture-exercised horses. More osteochondral lesions were detected in the ridden horses than in nonridden horses, and the lesions that were detected were of greater severity in the ridden horses. Findings also supported the hypothesis that higher his-topathologic scores would be found at sites predisposed to osteoarthritis in the CD joint than in sites not predisposed to osteoarthritis; however, in the TMT joint, scores were consistent over the whole surface. In addition, the hypothesis was supported that the shape and depth of the lesions would correlate with the cellular arrangement, the organization of the HC-CC and CC-SCB junctions, and the organization of the SCB.
The dorsomedial aspect of the CD joint and dorsolateral aspect of the TMT joint are areas subject to high mechanical loads relative to other locations in the tarsus.5–7,20 In the present study, dorsomedial lesions were detected in the CD joint and dorsolateral lesions were evident in the TMT joint, which may reflect the pattern of loading across the distal tarsal joints that has previously been described.5–7 These observed dorsal changes may have been attributable to dorsal compression in the joint while the horse was jumping or performing dressage movements. A medial-to-lateral load transfer was revealed by use of strain gauges in a group of ponies that were pasture exercised5 and was supported by bone modeling assessment by use of nuclear scintigraphy in horses with no history of hind limb lameness.6 However, load transfer may be different in horses that train in straight lines (eg, treadmill-trained horses), in which the SCB thickness pattern is more uniform across the tarsal joints,20 thereby potentially explaining, at least in part, the lack of detection of lesions at the same locations when a horse trains in straight lines. Horses used for sport and those at pasture reportedly have different loading patterns across the distal tarsal joints.21
Adjoining cavitation and hillock-type lesions were more common in groups L and E than in group P. It is possible that this observation relates to the rotational loading to which these sites are subjected,25 which could reflect the type of defect seen. This type of lesion might also be associated with the turning and circles that ridden horses perform, which may accentuate the rotational movement within the CD and TMT joints.6,20
In the present study, SCB histologic morphology was typical in all 3 exercise groups, except at the dorsomedial aspect of the CD joint and dorsolateral aspect of the TMT joint. Radiographic and histologic changes with increasing age in the CD joints of Icelandic horses26 and in Thoroughbreds27 have been described. In Icelandic horses, SCB sclerosis does not appear to be a primary factor in the development of osteoarthritis but is believed to be caused by uneven distribution of mechanical load throughout the joint.26 Areas of high load are the dorsomedial aspect of the CD joint and dorsolateral aspect of the TMT joint, and this is where abnormal SCB was evident in our study. However, in Thoroughbreds, changes in the SCB plate, joint junctions, and sclerotic SCB increase in severity with increasing age.27 The etiopathogenesis of osteoarthritis is not fully understood; however, there is likely to be a difference between the 2 breeds because osteoarthritis is hereditary in Icelandic horses.28
Lesions and higher histopathologic scores appeared to be correlated with ridden exercise in our study. It is possible that this phenomenon was related to the carriage of extra weight of the rider or altered loading patterns. The rider influences a horse's movement, undertaking specific maneuvers in dressage or jumping.29 Elite-level dressage horses need to perform sideways movements, turns around a single limb (pirouettes), and highly collected gaits (passage and piaffe), all of which require the tarsus to flex more than in other gaits.30 For an elite show jumper, the tarsus is under compression for a longer period on takeoff and landing. In the final stage of a jumping competition, a horse will also be required to perform tight turns and circles at high speed.31 All these factors could subject the tarsus to frequent, intense loading or compression for a greater proportion of each stride than with other horses,30,31 and such forces could theoretically lead to more histologic change.
Depth and shape of the lesions in the present study were correlated with cellular arrangement, organization of the HC-CC and CC-SCB junctions, and organization of the SCB. It is also possible that these features may reflect attempts to heal the lesions. Interestingly, the correlation between cellular arrangement and organization of the SCB was the only one to increase in strength (from weak to moderate) as exercise intensity increased. The altered organization of the SCB may have been an attempt of the cells to respond to changes in the structure and mechanical properties of the SCB. In humans, thickness and remodeling of SCB bone are influenced by intensity of the training and the degree of loading in the joint.32,33
When considering the results of our study, one should take into account the small sample size (10 joints/group). One should also consider that horses in the pasture-exercised group were raced at 2 years of age and that 2 horses in the elite competition group were not in elite-level work at the time they were euthanatized, having recently been restricted to box rest and controlled walking exercise. In addition, the results regarding the distal tarsal joints are not necessarily generalizable to other joints, particularly joints with different patterns of movement and loading. Any of these factors could have had an influence on the findings.
Regardless of these limitations, lesions were detected at a dorsomedial location in the CD joint and a dorsolateral location in the TMT joint, supporting these as sites at risk for developing osteoarthritis, potentially caused by osteochondral overloading at these locations. Furthermore, higher histologic grades were assigned to joints of ridden versus pasture-exercised horses and high-intensity versus low-intensity exercise, suggesting that as this loading increases and changes, there may be an increased risk of osteoarthritis formation at predisposed sites in distal tarsal joints of horses.
ABBREVIATIONS
| AC | Articular cartilage |
| CC | Calcified cartilage |
| CD | Centrodistal |
| HC | Hyaline cartilage |
| SCB | Subchondral bone |
| TMT | Tarsometatarsal |
Branch MV, Murray RC, Dyson SJ, et al. How does osteochondral structure change with age? (poster presentation). Trans 51st Meet Orthop Res Soc, Washington, DC, February 2005.
Branch MV, Murray RC, Dyson SJ. The effect of age on the structure of the equine distal tarsal osteochondral unit (abstr), in Proceedings. Br Equine Vet Assoc Cong 2004;298.
Biro UK, London, England.
CellPath PLC, Mochdre, Newtown, Powys, Wales.
Ralwax, VWR International Ltd, Poole, Dorset, England.
Bayer VIP, Newbury, Berkshire, England.
DPX, Raymond A Lamb Ltd, Eastbourne, East Sussex, England.
Olympus DP12 microscope, Olympus UK Ltd, London, England.
Analyse-it for Microsoft Excel, version 1.73, Analyse-it Software Ltd, Leeds, West Yorkshire, England.
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Appendix
Scoring system used for grading of histologic samples of cartilage and SCB.
| Characteristic | Score |
|---|---|
| Location of lesion | |
| No lesion | 0 |
| On 1 side of the joint | 1 |
| Adjoining or matching lesions (on adjacent joint surfaces) | 2 |
| Depth and shape of lesion | |
| Normal, even surface | 0 |
| a) Fissures within HC; b) irregular surface (fibrillation) | 1 |
| a) Fissures extending into CC; b) indentations and hillocks forming | 2 |
| a) V-shaped lesion extending through CC; b) partial fragmentation | 3 |
| a) Bite-shaped lesion extending through CC; b) fragmentation of AC | 4 |
| a) Fusion of bones; b) total collapse of joint | 5 |
| Cellular arrangement | |
| Typical cellular arrangement | 0 |
| Cellular rows becoming random | 1 |
| Random rows, chondrocyte clusters forming | 2 |
| Disorganized cellular arrangement, formation of chondrones | 3 |
| Large number of chondrones present | 4 |
| Cellular loss | 5 |
| Organization at HC-CC and CC-SCB junctions | |
| Clear, typical junction | 0 |
| Clear but clusters of cells merging with junction | 1 |
| Junction beginning to collapse, large number of disorganized cells | 2 |
| Junctions have totally collapsed, cellular loss beginning | 3 |
| Loss of junction, total cellular loss | 4 |
| Fusion of junctions | 5 |
| Organization of SCB | |
| Uniform, typical appearance | 0 |
| Bone space starting to enlarge | 1 |
| Cells present in bone spaces with smooth edges, mild fibrosis | 2 |
| Osteoclasts present in bone spaces with irregular edges, moderate fibrosis | 3 |
| Large bone spaces, marked fibrosis | 4 |
| Chaotic disorganization of cells, necrotic tissue present in bone spaces | 5 |
