Morphological, structural, and mechanical characteristics of SCB of the distal metacarpal condyles of Thoroughbred racehorses and their relationship with exercise history have been the focus of investigation in recent years.1-5 The anatomically related gradient in bone mineral density was recently described, and structural and mechanical characteristics of the SCB across the metacarpal condyles were determined by use of micro-CT and compressive in vitro mechanical testing.6,7 The distopalmar SCB of the MC3 in racing Thoroughbreds is denser, more robust, and stronger in the condyles than in the sagittal ridge. Sharp gradients of these properties have been found at the level of the condylar grooves and are believed to be implicated in the pathogenesis of condylar fractures.2,3,8,9
Bones are sensitive to their mechanical environment and respond by adapting their mass and their external and internal architecture to the mechanical requirements.10 For example, the pattern of TBB in the human femur and the sheep calcaneus closely follows principal stress and strain trajectories.10–12 Although this so-called trajectorial or Wolff theory has several limitations, the relationships between TBB microstructure and its mechanical usage have been reported.13,14 Instead of being homogeneously distributed and randomly oriented (isotropy) within a whole bone specimen, bone structural elements (trabeculae) are strategically positioned, conferring upon the bone its anisotropic characteristics: trabeculae are oriented along the principal directions of forces within the bone, making the bone stronger in that particular loading direction.11,12 Therefore, by studying the architectural characteristics of SCB in equine metacarpal condyles, it should be possible to infer, at least in part, the nature of the loads acting on the SCB at that location.
The anistropy of the SCB of the distal condylar area of the MC3 in racing Thoroughbreds can be easily appreciated at the macroscopic level.15 The SCB at this location appears highly organized with robust plates running parallel to the sagittal plane and with few mediolateral connections.16 This form of microstructural anisotropy appears to be more pronounced in horses with a longer racing history.17 Although the microstructure of the SCB is believed to give maximum strength and protection in the sagittal plane in which the bone rotates, it offers minimal resistance to proximal propagation of fracture in the sagittal plane.16 There also seems to be a parallel relationship between the anisotropic pattern of trabecular disposition and the characteristic anatomic course of distal condylar fractures of the MC3 in racing Thoroughbreds.16 Limited research evaluating SCB anisotropy at this location has been performed. Boyde et al16 evaluated the 3-D architecture of 2 beam-like samples of SCB and TBB obtained from a mediolateral dorsal slice (frontal plane) collected at the midpoint of the distal aspect of the condyle. The SCB within those beams had a high DA that was plainly evident via visual inspection. However, the distribution of load around the circumference of the condyles varies substantially during exercise and is dependent on the degree of flexion and extension of the joint.15 The palmar aspect of the metacarpal condyles supports most of the load during racing, and this is the location where major SCB changes occur, including SCB disease.1,3 Therefore, greater changes in SCB anisotropy may be expected at the palmar aspect of the metacarpal condyles, which could be relevant in the pathogenesis of clinical conditions such as traumatic osteoarthritis and condylar fractures.
Mean intercept length analysis is a 3-D stereological method that measures the orientation and anisotropy of porous media, such as TBB. The method is based on measuring the lengths of intersections of a regularly spaced parallel array of test lines with the trabecular structure. The array of test lines is realigned over many orientations, from which a fabric ellipsoid (3-D ellipse) is calculated.18,19 Structures with no preferred orientation are characterized by a spherical ellipsoid, while those with preferential alignment in one direction will have the major axis of the ellipsoid aligned with that direction. Stereological analyses are typically applied to 3-D images acquired by tomographic imaging systems. In particular, micro-CT represents the present gold standard for bone imaging and stereological analysis because it provides nondestructive, high-resolution 3-D images of bone architecture.20,21 Softwarea provides an implementation of the MIL method for analyzing digitally reconstructed 3-D images obtained by micro-CT. Micro-CT and software have been used to study the distopalmar SCB of the MC3 condyles.6
The objective of the study reported here was to determine the anisotropic characteristics of SCB micro-structure in the distopalmar aspect of the MC3 condyles in racing Thoroughbreds by applying the MIL method to 3-D micro-CT images. We hypothesized that the principal trabecular orientation and DA vary with anatomic location (condyles vs sagittal ridge and SCBP vs TBB) and with different stages of SCB disease.
Materials and Methods
Animals—One hundred twelve Thoroughbred racehorses underwent postmortem examination at the Ontario Veterinary College of the University of Guelph during the 2004 and 2005 racing meets.6 Both MC3s were collected from all horses and dissected free of tissues. The condylar region of each MC3 was examined by use of micro-CTb images acquired at 80 kV and 450 μM, with a 45-μm isotropic voxel resolution; corrected for fan-beam projection distortion and reconstructed into a 3-D format; and then imported into analysis software.a A dorsofrontal section (coincident with the loading direction of the condylar SCB against the PSB) was obtained from the SCB located at the distopalmar aspect of the condyles in an area representative of SCB changes.1,3 This area was located just palmar to the transverse ridge where there is a flattening of the condylar surface and corresponds to the contact area with the PSB during the stance phase of the gallop.1 Images were visually evaluated and classified according to category of bony changes, on a scale from 0 (normal) to 8 (condylar fracture).22 When several slices from each condyle were analyzed, the highest score assigned to the 2-D image (slice) with the most severe lesions of the condyle was considered as the condyle score. Then, each horse was assigned to the category corresponding to the maximal score assigned to the 4 condyles of both MC3s of the horse. Upon completion of micro-CT imaging, all MC3s were wrapped in gauze soaked in physiologic saline (0.9% NaCl) solution, placed inside 2 plastic bags, and stored at −20°C until analyzed.
Sample population—From the initial sample of 112 horses, the MC3s of 12 horses (24 MC3s) were selected and classified into 2 groups of 6 pairs of bones each, according to the assigned category of SCB disease.6 Group 1 (mild lesions) consisted of bones with sclerosis and mild focal or coalescing radiolucent areas in the SCB of the distopalmar aspect of the MC3 without involvement of the articular surface (categories 0, 1, and 2). These characteristics were considered representative of incipient maladaptive remodeling. Group 2 (severe lesions) consisted of bones with more severe multifocal radiolucent areas traversing the SCBP or affecting the articular surface (categories 5 to 7). These characteristics were considered representative of end-stage maladaptive remodelling. Horses with condylar fractures (category 8) were not included in the study
Specimen definition—For each MC3, 3 ROIs were defined at the sagittal ridge and the midpoint of each condyle. The ROIs were located at the distopalmar articular surface, corresponding to the contact area of the proximal sesamoid bones during the stance phase of the gallop,23 which also corresponds to the region where degenerative lesions develop.1 The articular cartilage was removed from the distopalmar articular condylar surface with a blade. At each ROI, samples were collected in a distopalmar-proximodorsal direction from the articular surface in an alignment consistent with the direction of the compressive force applied by the PSBs during maximal extension of the metacarpophalangeal joint during racing (Figure 1). At each ROI, 2 cubic specimens of bone approximately 6 × 6 × 6 mm were collected. The dimensions of the bone specimens were determined on the basis of the estimated thickness of the SCBP at each location.6 Specimens from the distal aspect of the bone were considered to include mostly the calcified cartilage layer and the SCBP, whereas specimens from the proximal aspect of the bone included mostly TBB. Specimen collection and acquisition of micro-CT images have been described in detail elsewhere.6
Illustration of the method and location of specimen collection in a study of subchondral microarchitecture of the distopalmar aspect of the MC3 in racing Thoroughbreds. A—Lateral view of the distal end of the MC3, indicating the distopalmar-dorsoproximal direction along which specimens were collected (simulating the loading direction against the PSBs). B—Dorsal view of the distal end of the MC3, indicating sites of specimen collection. D = Distal (SCBP). Do = Dorsal. L = Lateral. M = Medial. P = Proximal (TBB). Pa = Palmar. S = Sagittal. X = Width of medial condyle. Y = Width of lateral condyle.
Citation: American Journal of Veterinary Research 71, 10; 10.2460/ajvr.71.10.1148
Illustration of the method and location of specimen collection in a study of subchondral microarchitecture of the distopalmar aspect of the MC3 in racing Thoroughbreds. A—Lateral view of the distal end of the MC3, indicating the distopalmar-dorsoproximal direction along which specimens were collected (simulating the loading direction against the PSBs). B—Dorsal view of the distal end of the MC3, indicating sites of specimen collection. D = Distal (SCBP). Do = Dorsal. L = Lateral. M = Medial. P = Proximal (TBB). Pa = Palmar. S = Sagittal. X = Width of medial condyle. Y = Width of lateral condyle.
Citation: American Journal of Veterinary Research 71, 10; 10.2460/ajvr.71.10.1148
Illustration of the method and location of specimen collection in a study of subchondral microarchitecture of the distopalmar aspect of the MC3 in racing Thoroughbreds. A—Lateral view of the distal end of the MC3, indicating the distopalmar-dorsoproximal direction along which specimens were collected (simulating the loading direction against the PSBs). B—Dorsal view of the distal end of the MC3, indicating sites of specimen collection. D = Distal (SCBP). Do = Dorsal. L = Lateral. M = Medial. P = Proximal (TBB). Pa = Palmar. S = Sagittal. X = Width of medial condyle. Y = Width of lateral condyle.
Citation: American Journal of Veterinary Research 71, 10; 10.2460/ajvr.71.10.1148
Acquisition of micro-CT images—The 6 cubes of SCB collected from each MC3 were wrapped together in gauze soaked in saline solution and sealed with plastic film. Care was taken to ensure maintenance of the correct anatomic position and orientation of the cubes within the micro-CT gantry. The package of 6 cubes from each metacarpal bone was positioned above a calibration phantom and introduced into the gantry of the micro-CT scanner.b After image acquisition, scan data were corrected and CT values were calibrated into Hounsfield units by use of the calibration phantom.c The calibration phantom included a bubble filled with water, a piece of bovine hydroxyapatite, and a defect filled with air, so that Hounsfield unit values for water, bone, and air, respectively, could be determined. After calibration, full-resolution reconstruction of the 6 cubes of SCB from each MC3 was performed by use of user-defined 3-D ROIs.a The same investigator (LMRM), who was unaware of specimen group allocation, performed this procedure for all specimens.
Bone analysis—Each specimen of SCB was analyzed with advanced micro-CT bone analysis software.6,a Three-dimensional bone architecture was characterized for each sample by use of MIL measurements. The MIL method measures the orientation and anisotropy of the trabecular architecture by measuring the intersections of an array of parallel lines with the trabecular structure.18,19 On the basis of these measurements, the fabric ellipsoid defining the anisotropy of a sample of bone tissue is calculated. In particular, the 3 eigenvectors (e1; e2 and e3) defining the fabric ellipsoid of each block were calculated.
The x, y and z coordinates of the corners of each cubic sample within its 3-D micro-CT image were recorded. From these coordinates, the 3 anatomic vectors (proximodistal, dorsopalmar, and mediolateral) of each sample were calculated. Orthogonality of the 3 mutually perpendicular vectors was mathematically enforced by the Gram-Schmidt process. From these measurements, the following output variables were calculated: the angle (θ) between the principal direction (e1) of the trabecular microstructure and the anatomic dorsoproximal-distopalmar direction along which samples were cut (in other words, on what angle e differs from the sagittal plane) and the DA (|e1|/|e3|) defined as the ratio of the lengths of the maximum and minimum eigenvectors of the fabric ellipsoid.
Statistical analysis—Normality of the data was assessed, and a statistical analysis was performed by use of a factorial design within a partial randomized block ANOVA. Horse was considered as a block, and factors investigated included group (group 1 vs group 2), side (left vs right), level (TBB vs SCBP), and ROI (medial condyle, lateral condyle, and sagittal ridge). When appropriate, paired comparisons were based on a Tukey adjustment. For all comparisons, P ≤ 0.05 was considered significant.
Results
The 12 horses included in the study had a median age of 4 years (range, 2 to 7 years). Median and range of age for horses in groups 1 and 2 were 3 years (2 to 4 years) and 5.5 years (4 to 7 years), respectively. Group 1 included 1 sexually intact male, 2 castrated males, and 3 females; group 2 included 3 castrated males and 3 females. Other characteristics of the 12 horses and examples of micro-CT images of both groups have been reported.6
No side effect (left vs right) was found for any of the variables in the study. Overall, a mild ROI effect was detected with DA (Table 1); however, no significant differences were found. Conversely, level had a significant (P < 0.001) effect; TBB (mean ± SE DA, 1.754 ± 0.043) was significantly (P < 0.001) more anisotropic than SCBP (mean ± SE DA, 1.289 ± 0.043).
Mean (95% confidence interval) values of the angle θ (the angle between the principal direction of the trabecular microstructure of the MC3 and the anatomic dorsoproximal-distopalmar direction along which specimens were obtained) and mean ± SE values of DA (the ratio of the lengths of the maximum and minimum eigenvectors of the fabric ellipsoid) in 12 MC3 pairs from racing Thoroughbreds.
| ROI | Angle θ | DA |
|---|---|---|
| Lateral condyle | 9.021 (7.463-10.904) | 1.474 ± 0.045 |
| Medial condyle | 8.837 (7.299-10.698) | 1.536 ± 0.045 |
| Sagittal ridge | 40.669 (33.644-49.162)* | 1.553 ± 0.045 |
Significantly (P < 0.001) different from θ values for lateral and medial condyles, via ANOVA with ROI as a factor. Values of DA were not significantly (P = 0.056) different.
When DA of TBB was compared between groups, group 1 had significantly greater DA (mean ± SE, 1.855 ± 0.060) than did group 2 (1.652 ± 0.060). No significant difference between groups was detected for SCBP (group 1, 1.285 ± 0.06; group 2, 1.293 ± 0.06). However, when ROI was taken into account, significant differences between the TBB and SCBP were observed in all 3 ROIs (Table 2). In the TBB, the DA was greater in the medial condyle of group 1 than in the medial condyle of group 2, although the difference did not quite reach significance (P = 0.059). In both groups, no differences were found between condylar and sagittal ridge samples with the exception of group 2 in which the TBB of the lateral condyle was significantly (P = 0.014) less anisotropic than the TBB of the sagittal ridge.
Results of ANOVA (mean ± pooled SE) for the interaction group*level*ROI for the variable DA in the same specimens as in Table 1.
| Variable | P value | Level | Group 1 | Group 2 | ||||
|---|---|---|---|---|---|---|---|---|
| Lateral | Sagittal | Medial | Lateral | Sagittal | Medial | |||
| DA | 0.029 | TBB | 1.788 ± 0.072 | 1.866 ± 0.072 | 1.909 ± 0.072 | 1.554 ± 0.072 | 1.783 ± 0.072 | 1.621 ± 0.072 |
| SCBP | 1.253 ± 0.072 | 1.324 ± 0.072 | 1.279 ± 0.072 | 1.303 ± 0.072 | 1.240 ± 0.072 | 1.335 ± 0.072 | ||
The angle between the principal eigenvector and the sagittal plane was significantly (P < 0.001) smaller in condylar samples than in sagittal samples (factor ROI; Table 1). With medial and lateral condyle samples, no side dependence on angle was observed for SCBP and TBB samples (Table 3). The angle value was smaller for TBB (13.705°) than SCBP (15.982°), but the difference was not significant. The interaction level X ROI was significant (P < 0.001), and the significant difference was at the sagittal ridge, where SCBP had a greater angle than did TBB. At the condyles, the angle was larger for TBB than for SCBP, but differences were not significant.
Results of ANOVA (mean [95% confidence interval] for angle θ; mean ± pooled SE for DA) for the interaction level*ROI in the same specimens as in Table 1.
| Variable | P value | Level | ROI | ||
|---|---|---|---|---|---|
| Lateral | Sagittal | Medial | |||
| Angle θ | < 0.001 | TBB | 10.596 (8.343-13.457)a | 24.826 (19.454-31.682)*b | 9.7871 (7.706-12.431)a |
| SCBP | 7.68 (6.018-9.801)a | 66.623 (52.456-84.618)b | 7.978 (6.223-10.229)a | ||
| DA | 0.096 | TBB | 1.671 ± 0.051 | 1.825 ± 0.051 | 1.765 ± 0.051 |
| SCBP | 1.278 ± 0.051 | 1.282 ± 0.051 | 1.307 ± 0.051 | ||
Significantly (P < 0.001) different from value for the sagittal ridge in the SCBP.
Within each level, values with different superscript letters are significantly (P < 0.05) different.
Discussion
Results indicated that the SCB at the distopalmar aspect of the MC3 of a select population of Thoroughbred racehorses from 2 Ontario racetracks that were euthanatized for diverse reasons was anisotropic and that the anisotropic characteristics varied according to specific anatomic location and were related to the severity of SCB disease. Within the condyles, trabeculae were highly ordered and aligned nearly parallel to the sagittal plane, in agreement with observations in another study.16 However, trabeculae in the sagittal ridge were more obliquely oriented, especially at the distal level. On the basis of the trajectorial relation of trabecular microstructure with mechanical usage,13 findings indicated that joint loading was transmitted primarily through the condyles and less through the sagittal ridge and there were significant differences in the trajectories of functional loads in the SCB across the metacarpal condyles. Sharp changes in load trajectories at the condylar grooves could contribute to the pathogenesis of condylar fractures, with hypothetical tensile forces occurring between the sagittal ridge and the condyles.
According to the Poisson effect, when a material is subjected to a compressive force (like the weight down the limb through the distal MC3 condyles against the PSBs), the material contracts along the loading direction (proximal to distal) and expands in the transverse direction (lateromedial and dorsopalmar). Because of the curvature of the proximal surface of the first phalanx and the suspensory apparatus at the palmar aspect, expansion along the dorsopalmar direction is likely more restricted than along the lateromedial direction. Therefore, we hypothesize that the distal condyles may be subjected to a cyclic expansion in a lateromedial direction. It has been reported that initial fatigue failure of the SCB usually localizes at the transition between the dense condylar SCB and the less dense SCB at the sagittal ridge,3 affecting the calcified cartilage and the immediate SCBP.24 These 2 layers constitute a cortical shell that surrounds the deeper TBB. Therefore, we further hypothesize that once a defect is present in the cortical shell, and if chronic loading is sustained, causing repeated lateromedial expansions of the MC3 condylar SCB, tensile forces would arise in the subsequent propagation of the defect in a proximal direction. In this situation, and as it has been suggested on the basis of the common fracture configuration,16 fracture propagation parallel to the trabeculae would represent the least resistive pathway, requiring breakdown of thin bridges or connections between the plate-like trabeculae, following a zipper-like effect.
The DA provides insight into the directional dependence of bone strength.19,25 Trabeculae are often oriented parallel with the dominant loading direction to increase bone strength. Consequently, TBB has strongly anisotropic characteristics where such loading prevails.13 Although both tissue layers (SCBP and TBB) in this study had anisotropy to some extent, the SCBP was less anisotropic than the TBB. The more isotropic microstructure of the SCBP can be explained by a higher degree of sclerosis as evidenced by an increase in bone volume fraction caused by the narrowing and filling in of marrow spaces.16 As described by Boyde et al,16 the presence of sclerosis reduces the anisotropy of the trabecular architecture in the SCBP samples, whereas the less sclerotic TBB still has strongly anisotropic characteristics. The suggested hypothetical transverse tensile forces acting at this location, as a result of lateromedial deformation caused during loading, could also be stimulating adaptation toward a more isotropic structure by inducing deposition of new bone transversly and reducing the preferrential proximodistal orientation of trabeculae.
Compared with group 1, the TBB in group 2 was less anisotropic, which was similar to previous observations that the TBB in group 2 had higher bone density (apparent and mineral) than group 1.6 These changes were likely the result of the adaptive response to higher strains transmitted to the TBB in the presence of underlying SCBP that was more deteriorated in group 2, compared with group l.26 Consequently, the decrease in anisotropy in the TBB in group 2, compared with group 1, would be indicative of bone failure in the SCBP samples of group 2.24 As bone failure accumulates in the SCBP, its capacity for load absorption decreases, leading to a greater proportion of the load being transferred to the TBB, which in turn sustains higher strain.26 Such an increase in strain will cause a greater adaptive response in the TBB, with new bone being deposited, filling in the former marrow cavities16 and leading to a less anisotropic structure.
The DA did not differ significantly between groups when each ROI (medial condyle, lateral condyle, and sagittal ridge) was compared separately. A greater proportion of osteoarthritic lesions occur in the medial condyle, compared with the lateral condyle.27 Also, a significant decrease in trabecular thickness was seen in the medial condyle SCBP of specimens with severe SCB lesions in comparison with the lateral condyle.6 These findings could be the result of a greater adaptive response in the medial condyle, in response to a greater proportion of the load being transmitted through the medial aspect of the forelimb. We did not find significant differences in this study to further support those findings, but the difference in anisotropy at the medial condylar TBB between groups was not large. Though speculative, the lack of significance could have been associated with the limited number of samples. Further research involving a larger population of horses is needed.
The lateral condyles of group 2 were less anistropic than the TBB in the sagittal ridge. Although the TBB in the medial condyles had lower anisotropy than the TBB in the sagittal ridge, the difference was not significant. This finding parallels the higher connectivity observed in the lateral condyle TBB,6 and both could be the result of higher stresses on the lateral versus medial condyle because of the smaller size of the lateral condyle and the higher slope of its articular surface.2,28
Highly ordered, sagittally oriented trabeculae within the condyles of the MC3 support the concept that joint loading is primarily transmitted through the condyles and not the sagittal ridge, where trabeculae are oriented more obliquely. Adaptation of SCB to sharp changes in the trajectories of functional loads with hypothetical tensile forces at the condylar grooves might contribute to the pathogenesis of condylar fractures. The decrease in anisotropy of TBB observed in advanced stages of SCB disease is likely the result of an adaptive process.
Abbreviations
| DA | Degree of anisotropy |
| MC3 | Third metacarpal bone |
| Micro-CT | Micro-computed tomography |
| MIL | Mean intercept length |
| PSB | Proximal sesamoidean bone |
| ROI | Region of interest |
| SCB | Subchondral bone |
| SCBP | Subchondral bone plate |
| TBB | Trabecular bone |
MicroView ABA, version 2.1.2, GE Healthcare, London, ON, Canada.
GE Medical Systems eXplore Locus Micro CT Scanner, GE Medical Systems, London, ON, Canada.
SB3, Gammex RMI, Middleton, Wis.
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