Subchondral bone, which is composed of SCBP and SCTB, serves to maintain joint shape and is responsible for most of the biomechanical stress absorption on joints, sparing the overlying articular cartilage from damage.1–3 The SCBP is the dense layer of bone between the calcified cartilage and marrow spaces and is responsible for supporting articular cartilage.3,4 Subchondral trabecular bone is found immediately deep to the SCBP, which it supports, and is more compliant than cortical bone, allowing for deformation under joint loading and therefore dissipation of energy.3 When under mechanical stress, subchondral bone adaptively responds by modeling and remodeling5 to become more mechanically functional.6 When an imposed strain is greater than the maximum strain threshold, bone tissue is added for increased strength.7 This phenomenon has been demonstrated in racing Thoroughbreds, in which the third carpal subchondral bone is reportedly denser in trained versus untrained horses.8
Pauwels9 first showed that the primary stress on a joint influences the underlying bone density in that joint. More recently, CT osteoabsorptiometry has been used to determine subchondral bone density patterns, which are believed to reflect long-term stress upon a joint.10 These patterns, from which the loading history of articular surfaces can be inferred, have been identified in healthy hip and elbow joints in humans,11,12 elbow joints in dogs,13,14 and the distal portion of the metacarpus in horses.15–17 Subchondral bone densities and mechanical properties of the distal portion of the femur have been determined in dogs and horses to characterize appropriate donor and recipient sites for autologous osteochondral transplantation.18,19 In horses, osteochondral cores from 9 ROIs on the MFC were used to extrapolate a map of the subchondral bone density patterns and mechanical properties in the MFC. Horse breed, purpose, or distal femoral laterality was not taken into account.18 The purpose of the study reported here was to map the subchondral bone density patterns in MFCs of Thoroughbred racehorses and determine whether MFC morphometrics and subchondral bone density patterns differed between left and right limbs.
Materials and Methods
Acquisition of specimens—Left and right stifle joints from 6 Thoroughbred racehorses that were euthanized because of catastrophic forelimb breakdowns (n = 4) or respiratory (1) or cardiovascular disease (1) at a racetrack were used in the study. The horses ranged in age from 2 to 8 years and included 3 geldings, 1 mare, 1 stallion, and 1 unidentified horse.
Both stifle joints from 4 horses were harvested from the midaspect of the femur to the midaspect of the tibia. The femoropatellar and femorotibial joints were disarticulated and the soft tissues removed. The distal third of each femur was harvested with a band saw to sever the distal portion. Gross appearance of condylar surfaces was graded by a board-certified equine surgeon (CEK) for cartilage and subchondral bone pathological lesions (Appendices 1 and 2). The specimens were subsequently placed in a water bath, with condylar orientation mimicking right lateral recumbency.
Both hind limbs from 2 additional horses were disarticulated at the coxofemoral joint because of use in another study. The hind limbs were placed in the CT bore individually, mimicking right lateral recumbency with soft tissues intact. After the CT scan, the femoropatellar and femorotibial joints were disarticulated, the soft tissues were removed from the distal portion of the femur, and the condylar surfaces were graded by the same board-certified equine surgeon. Differences in the 2 harvesting techniques were deemed negligible because a previous study20 of equine metacarpi showed that evaluation of bone densities via CT is not influenced by whether intact or disarticulated joints are used.
CT—Computed tomography was performed with a commercially available scanner.a Left and right specimens from 5 horses were scanned at 140 kV and 177 mA, with a slice thickness of 1 mm and frontal slice orientation. Left and right stifle joints from the remaining horse were also analyzed. For that horse, because of its use in another study, the distal portion of the left femur was scanned at 140 kV and 221 mA, with a slice thickness of 0.8 mm, and the right distal femur was scanned at 140 kV and 278 mA, with a slice thickness of 0.8 mm. The unprocessed CT data were then uploaded into a custom-written analysis programb,c that allowed for specimen alignment, morphometric analysis, and bone density measurement.
To minimize the effects of any differences in scan settings and to represent subchondral bone as a density, a dipotassium phosphate phantom was scanned with identical settings prior to scanning each individual specimen. A best-of-fit linear regression model was created for each specimen and its corresponding phantom scan to convert all in HUs from each individual specimen into dipotassium phosphate–equivalent densities (mg/mL).21
Alignment was achieved in 3 planes. The frontal and sagittal planes were established cranially at the transition of the MFC and the medial trochlear ridge and caudally at the most proximal aspect of the caudal portion of the MFC. Specifically, the frontal and sagittal planes were established perpendicular and parallel to this axis, respectively. The transverse plane was established parallel to the most distal points of the medial and lateral femoral condyles. The CSC was determined to be 375 HUs for all analyses. This value was determined on the basis of volumetric calculation of the mean of 50 HUs for cartilage and 800 HUs, representing an estimated mean SCBP density of the MFCs.
Morphometrics—All morphometrics were established from the alignment axis. The width of each MFC was derived at the widest point of the MFC on the alignment axis in the frontal plane. Height was derived from the midpoint of the width line in the frontal plane and spanned from the sagittal alignment axis to the distal CSC of the MFC. Length was derived from the midpoint of the MFC width line and determined to be the longest distance between the cranial and caudal aspects of the MFC in the sagittal plane.
Five frontal slices and 3 sagittal slices were generated from the center point of each MFC, which was identified as the intersection of the frontal, sagittal, and transverse planes. The 5 frontal planes (cranial second slice, cranial first slice, frontal midslice, caudal first slice, and caudal second slice) were derived at 16.7%, 33.3%, 50.0%, 66.7%, and 83.3% of the length line, respectively (Figure 1). The 3 sagittal planes (abaxial slice, midsagittal slice, and axial slice) were derived at 25.0%, 50.0%, and 75.0% of the width line, respectively.
Locations of frontal CT slices (A) of equine MFCs with the cranial second slice (CRA2), cranial first slice (CRA1), frontal midslice (MID), caudal first slice (CAU1), and caudal second slice (CAU2) located at 16.7%, 33.3%, 50.0%, 66.7%, and 83.3% of the MFC length from cranial to caudal, respectively, and of sagittal slices (B) with the abaxial slice (ABA), midsagittal slice (MID), and axial slice (AX) located at 25.0%, 50.0%, and 75.0% of the MFC width from abaxial to axial, respectively. Cranial is at the top.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Locations of frontal CT slices (A) of equine MFCs with the cranial second slice (CRA2), cranial first slice (CRA1), frontal midslice (MID), caudal first slice (CAU1), and caudal second slice (CAU2) located at 16.7%, 33.3%, 50.0%, 66.7%, and 83.3% of the MFC length from cranial to caudal, respectively, and of sagittal slices (B) with the abaxial slice (ABA), midsagittal slice (MID), and axial slice (AX) located at 25.0%, 50.0%, and 75.0% of the MFC width from abaxial to axial, respectively. Cranial is at the top.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Locations of frontal CT slices (A) of equine MFCs with the cranial second slice (CRA2), cranial first slice (CRA1), frontal midslice (MID), caudal first slice (CAU1), and caudal second slice (CAU2) located at 16.7%, 33.3%, 50.0%, 66.7%, and 83.3% of the MFC length from cranial to caudal, respectively, and of sagittal slices (B) with the abaxial slice (ABA), midsagittal slice (MID), and axial slice (AX) located at 25.0%, 50.0%, and 75.0% of the MFC width from abaxial to axial, respectively. Cranial is at the top.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Each frontal slice was analyzed as thirds (abaxial section, midsection, and axial section) and halves (abaxial half and axial half). The abaxial section spanned 30° to 70° from the center point of the MFC, and the midsection, axial section, abaxial half, and axial half sections spanned 70° to 110°, 110° to 150°, 30° to 90°, and 90° to 150° from the center point of the MFC, respectively (Figure 2).
Depiction of regions of CT frontal slices that were analyzed as thirds (abaxial section, middle section, and axial section) and halves (abaxial and axial) for SCBP (A) and SCTB (B) measurements in MFCs from Thoroughbred racehorse cadavers. The abaxial section spanned 30° to 70° from the center point of the MFC, and the middle section, axial section, abaxial half, and axial half sections spanned 70° to 110°, 110° to 150°, 30° to 90°, and 90° to 150° from the center point of the MFC, respectively. Axial is to the left.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Depiction of regions of CT frontal slices that were analyzed as thirds (abaxial section, middle section, and axial section) and halves (abaxial and axial) for SCBP (A) and SCTB (B) measurements in MFCs from Thoroughbred racehorse cadavers. The abaxial section spanned 30° to 70° from the center point of the MFC, and the middle section, axial section, abaxial half, and axial half sections spanned 70° to 110°, 110° to 150°, 30° to 90°, and 90° to 150° from the center point of the MFC, respectively. Axial is to the left.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Depiction of regions of CT frontal slices that were analyzed as thirds (abaxial section, middle section, and axial section) and halves (abaxial and axial) for SCBP (A) and SCTB (B) measurements in MFCs from Thoroughbred racehorse cadavers. The abaxial section spanned 30° to 70° from the center point of the MFC, and the middle section, axial section, abaxial half, and axial half sections spanned 70° to 110°, 110° to 150°, 30° to 90°, and 90° to 150° from the center point of the MFC, respectively. Axial is to the left.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Each sagittal slice was analyzed as quarters (cranial second section, cranial first section, caudal first section, and caudal second section) and halves (cranial half and caudal half). The cranial second section spanned 0° to 45° from the center point of the MFC, and the cranial first section, caudal first section, caudal second section, cranial half, and caudal half sections spanned 45° to 90°, 90° to 135°, 135° to 180°, 0° to 90°, and 90° to 180° from the center point of the MFC, respectively.
A curvature measurement (spline) was generated along the CSC from each of the sections and recorded as a radius in millimeters. Only the convex aspects of the MFC were measured. When curvature was concave, no measurement was recorded.
SCBP and SCTB densities—Subchondral bone plate density was generated from each of the sections. Regions of interest were created representing an area spanning from the CSC to 3 mm deep to the CSC for each section (Figure 2). Subchondral trabecular bone density was generated from each of the sections. Regions of interest were created, representing an area spanning from the CSC to 10 mm deep to the CSC for each section. The mean HUs for each SCBP and SCTB section were calculated and converted to a dipotassium phosphate equivalent density with the best-of-fit linear regression model developed for each specimen.
Statistical analysis—Repeatability of measurements was assessed by performing the alignment and morphometric and density analyses on the same specimen 3 consecutive times. All morphometric measurements had a coefficient of variation < 12%, and all density measurements had a coefficient of variation < 6%, so all morphometric and density measurements were deemed repeatable. The assumption of normal data distribution was evaluated separately for the difference (left limb vs right limb) in spline, SCBP density, and SCTB density measurements through Shapiro-Wilk testing. Variables with nonnormally distributed data were analyzed with the Wilcoxon signed rank test for paired data.
Medial femoral condyle width, length, height, and spline; SCBP density; and SCTB density measurements were compared between left and right MFCs in the frontal and sagittal planes with the paired t test.d In each plane, comparisons were made within slice and section. In the frontal plane, slices included cranial second slice, cranial first slice, frontal midslice, caudal first slice, and caudal second slice, and sections in each slice were abaxial section, middle section, axial section, abaxial half, and axial half. In the sagittal plane, slices included abaxial slice, midsagittal slice, and axial slice, and sections in each slice were cranial second section, cranial first section, caudal first section, caudal second section, cranial half, and caudal half. Values of P ≤ 0.05 were considered significant for all analyses.
Results
All horses had some degree of gross condylar pathological change. One specimen had no cartilaginous defects; however, softening and discoloration of articular cartilage were seen. All other specimens had partial- or full-thickness cartilage defects. The left and right MFCs from 1 horse had full-thickness defects of the subchondral bone. A subchondral bone cyst was grossly evident on the left MFC of that horse. Although a full-thickness erosion of the right MFC was also visible, a subchondral bone cyst in that area could only be identified via CT analysis.
Values for all variables were normally distributed, with the following exceptions: difference (left limb vs right limb) in spline for the axial half section of the caudal first slice and the abaxial half section of the cranial first slice, in SCBP for the abaxial and abaxial half sections of the caudal second slice and the abaxial section of the cranial second slice, in SCTB for the abaxial and abaxial half sections of the caudal second slice and the midsection of frontal midslice, in spline for the cranial first section and cranial second section of the axial slice, in SCBP for the caudal half section of the abaxial slice, and in SCTB for the cranial first section of the abaxial slice, the caudal first section of the axial slice, and the cranial second section of the frontal midslice. These variables were analyzed with the Wilcoxon signed rank test.
No significant differences in MFC width, length, or height between left and right limbs were identified (Table 1). The left MFC had significantly less curvature (greater spline) than the right at 2 ROIs. At the cranioaxial aspect in the frontal plane (axial half section of the cranial second slice; Table 2), the left spline was 2.74 mm greater than the right. At the midcaudal aspect in the sagittal plane (caudal second section of the midsagittal slice; Table 3), the left spline was 0.66 mm greater than the right. No other significant differences between left and right morphometrics were recorded.
Mean ± SD width, height, and length (mm) of MFCs in both hind limbs from 6 Thoroughbred racehorses.
| Condyle dimension | Left | Right |
|---|---|---|
| Width | 44.0 ± 2.1 | 42.7 ± 1.8 |
| Height | 35.1 ± 1.1 | 34.4 ± 1.4 |
| Length | 69.7 ± 1.6 | 69.2 ± 1.8 |
Mean ± SD spline measurements and SCBP and SCTB densities in various sections of the distal portion of the femurs from 6 Thoroughbred racehorses analyzed in the frontal plane via CT.
| Variable | Limb | Abaxial third | Middle third | Axial third | Abaxial half | Axial half |
|---|---|---|---|---|---|---|
| Cranial second-quarter slice | ||||||
| Spline (mm) | Left | 13.7 ± 2.8 | 39.2 ± 1.0a | 26.3 ± 7.4b | 14.8 ± 1.3b | 25.1 ± 4.6b* |
| Right | 14.1 ± 2.2 | 42.8c | 24.4 ± 6.8 | 14.6 ± 0.8b | 22.4 ± 4.3b | |
| SCBP (mg/cm2) | Left | 634.2 ± 93.5 | 789.1 ± 78.3 | 729.7 ± 72.1 | 685.4 ± 87.2 | 744.1 ± 67.9 |
| Right | 611.2 ± 87.5 | 798.4 ± 83.2 | 739.1 ± 109.5 | 671.7 ± 77.0 | 756.0 ± 98.5 | |
| SCTB (mg/cm2) | Left | 544.2 ± 84.9 | 654.6 ± 105.3 | 636.7 ± 103.5 | 579.0 ± 91.9 | 640.0 ± 99.4 |
| Right | 524.3 ± 67.1 | 638.1 ± 71.4 | 614.6 ± 86.5 | 559.1 ± 62.6 | 622.4 ± 82.7 | |
| Cranial first-quarter slice | ||||||
| Spline (mm) | Left | 18.3 ± 2.9 | 36.5 ± 1.7b | 52.4 ± 8.1 | 19.3 ± 1.1 | 30.9 ± 4.5 |
| Right | 19.0 ± 3.4 | 36.3 ± 8.1d | 58.1 ± 11.5 | 19.3 ± 1.6 | 32.3 ± 5.3 | |
| SCBP (mg/cm2) | Left | 608.8 ± 85.4 | 777.4 ± 79.3 | 671.9 ± 56.2 | 679.2 ± 76.1 | 693.7 ± 58.6 |
| Right | 572.1 ± 73.0 | 789.1 ± 67.7 | 707.4 ± 68.5 | 654.4 ± 60.7 | 723.4 ± 58.9 | |
| SCTB (mg/cm2) | Left | 564.2 ± 79.8 | 652.0 ± 85.2 | 586.6 ± 68.2 | 605.0 ± 79.1 | 597.7 ± 73.0 |
| Right | 552.9 ± 70.0 | 651.3 ± 64.1 | 583.5 ± 65.4 | 596.6 ± 69.6 | 594.4 ± 59.1 | |
| Frontal midslice | ||||||
| Spline (mm) | Left | 18.1 ± 2.5 | 34.4 ± 4.5b | 58.6c | 19.8 ± 2.3 | 43.0 ± 6.6 |
| Right | 17.3 ± 2.7 | 35.9 ± 5.5 | — | 19.5 ± 1.5 | 38.6 ± 7.9 | |
| SCBP (mg/cm2) | Left | 556.6 ± 71.2 | 770.4 ± 66.2 | 796.0 ± 62.3 | 656.6 ± 59.7 | 766.9 ± 59.8 |
| Right | 530.7 ± 73.0 | 758.4 ± 84.5 | 840.5 ± 80.9† | 637.7 ± 55.8 | 808.3 ± 61.4† | |
| SCTB (mg/cm2) | Left | 555.7 ± 58.9 | 653.2 ± 59.7 | 654.5 ± 49.9 | 605.7 ± 53.7 | 640.0 ± 51.8 |
| Right | 553.9 ± 72.2 | 664.7 ± 50.9 | 669.7 ± 59.4 | 606.9 ± 64.8 | 654.6 ± 51.2 | |
| Caudal first-quarter slice | ||||||
| Spline (mm) | Left | 16.3 ± 2.3 | 41.4 ± 18.3 | — | 17.8 ± 1.0 | 76.0 ± 42.8 |
| Right | 16.6 ± 2.7 | 36.1 ± 3.9 | — | 18.4 ± 1.9 | 59.4 ± 16.2 | |
| SCBP (mg/cm2) | Left | 518.0 ± 89.2 | 755.7 ± 27.0 | 689.4 ± 46.4 | 627.4 ± 65.2 | 704.2 ± 38.2 |
| Right | 489.4 ± 82.3 | 769.4 ± 50.5 | 749.6 ± 57.1‡ | 608.6 ± 72.8 | 751.1 ± 38.0† | |
| SCTB (mg/cm2) | Left | 515.3 ± 73.2 | 641.1 ± 29.3 | 553.6 ± 27.4 | 584.1 ± 73.6 | 575.7 ± 25.0 |
| Right | 503.4 ± 79.1 | 655.9 ± 55.7 | 585.6 ± 50.1† | 573.3 ± 75.0 | 603.5 ± 44.6 | |
| Caudal second-quarter slice | ||||||
| Spline (mm) | Left | 14.2 ± 3.1 | 46.0 ± 9.8 | 30.2 ± 7.6a | 16.0 ± 2.6 | 81.3 ± 39.5 |
| Right | 15.8 ± 4.5 | 46.2 ± 10.7 | 30.3 ± 0.6a | 15.6 ± 2.4 | 52.2 ± 16.3 | |
| SCBP (mg/cm2) | Left | 572.0 ± 103.9 | 797.6 ± 51.2 | 732.4 ± 62.8 | 672.8 ± 64.7 | 753.3 ± 51.7 |
| Right | 540.0 ± 91.7 | 828.4 ± 38.2 | 816.2 ± 81.5† | 648.5 ± 65.7 | 828.5 ± 66.5† | |
| SCTB (mg/cm2) | Left | 529.8 ± 68.2 | 663.8 ± 28.7 | 619.4 ± 27.0 | 588.9 ± 46.0 | 633.3 ± 13.9 |
| Right | 513.3 ± 67.9 | 723.9 ± 82.2 | 695.9 ± 95.0 | 579.5 ± 59.5 | 685.1 ± 51.0† | |
Spline is significantly (P ≤ 0.05) flatter than corresponding contralateral spline.
Significantly (P ≤ 0.05) denser than corresponding contralateral ROI.
Significantly (P < 0.01) denser than corresponding contralateral ROI.
— = All data points were concave, and there was no recording.
Two convex data points recorded.
Five convex data points recorded.
One convex data point recorded (and therefore no SD is given).
Four convex data points recorded.
Mean ± SD spline measurements and SCBP and SCTB densities in various sections of the distal portion of the femurs from 6 Thoroughbred racehorses analyzed in the sagittal plane via CT.
| Variable | Limb | Cranial second quarter | Cranial first quarter | Caudal first quarter | Caudal second quarter | Cranial half | Caudal half |
|---|---|---|---|---|---|---|---|
| Abaxial slice | |||||||
| Spline (mm) | Left | 26.6 ± 2.7 | 45.9 ± 8.1 | 39.9 ± 2.8 | 27.7 ± 10.1 | 31.0 ± 2.0 | 27.4 ± 2.9 |
| Right | 25.9 ± 3.2 | 44.9 ± 3.7 | 40.0 ± 2.6 | 24.8 ± 5.1 | 30.5 ± 1.6 | 28.0 ± 2.3 | |
| SCBP (mg/cm2) | Left | 524.7 ± 57.3 | 748.8 ± 86.3 | 670.9 ± 71.8 | 513.5 ± 99.3 | 632.5 ± 62.7 | 599.9 ± 77.6 |
| Right | 530.5 ± 70.4 | 741.9 ± 71.7 | 665.2 ± 104.8 | 500.9 ± 109.1 | 635.3 ± 63.6 | 590.1 ± 104.4 | |
| SCTB (mg/cm2) | Left | 495.2 ± 63.6 | 650.0 ± 88.9 | 594.1 ± 64.4 | 477.3 ± 65.0 | 570.8 ± 71.8 | 540.7 ± 61.7 |
| Right | 484.8 ± 60.4 | 650.1 ± 72.8 | 609.1 ± 90.8 | 468.1 ± 88.7 | 566.1 ± 63.5 | 539.3 ± 90.3 | |
| Midsagittal slice | |||||||
| Spline (mm) | Left | 35.6 ± 5.8 | 50.0 ± 5.7 | 42.6 ± 3.6 | 36.8 ± 1.8* | 37.9 ± 1.6 | 33.8 ± 1.5 |
| Right | 34.8 ± 6.3 | 54.6 ± 7.0 | 43.5 ± 2.5 | 36.2 ± 1.6 | 37.8 ± 2.3 | 33.4 ± 0.8 | |
| SCBP (mg/cm2) | Left | 596.2 ± 82.8 | 778.2 ± 86.5 | 810.6 ± 52.3 | 858.3 ± 32.0 | 678.2 ± 79.1 | 835.9 ± 38.3 |
| Right | 590.7 ± 65.8 | 778.0 ± 65.3 | 823.3 ± 29.8 | 889.9 ± 29.0 | 675.7 ± 60.2 | 858.5 ± 25.1 | |
| SCTB (mg/cm2) | Left | 548.4 ± 105.9 | 651.9 ± 76.6 | 664.2 ± 26.5 | 671.2 ± 26.9 | 595.1 ± 87.3 | 667.7 ± 24.8 |
| Right | 524.1 ± 58.7 | 646.1 ± 54.5 | 679.0 ± 43.9 | 687.9 ± 34.1 | 579.4 ± 54.0 | 683.6 ± 37.8 | |
| Axial slice | |||||||
| Spline (mm) | Left | 67.0 ± 51.4 | 97.1 ± 83.0 | 60.0 ± 21.1 | 27.3 ± 2.7 | 57.4 ± 13.2 | 31.6 ± 1.7 |
| Right | 53.4 ± 17.3 | 57.9 ± 11.6 | 53.8 ± 8.5 | 27.1 ± 1.5 | 52.3 ± 6.0 | 31.3 ± 0.7 | |
| SCBP (mg/cm2) | Left | 623.2 ± 73.0 | 658.1 ± 69.9 | 740.2 ± 53.1 | 710.9 ± 80.4 | 638.3 ± 70.4 | 723.2 ± 33.4 |
| Right | 625.5 ± 80.4 | 671.0 ± 62.1 | 766.4 ± 46.5‡ | 781.3 ± 46.5† | 645.9 ± 70.1 | 773.7 ± 30.2‡ | |
| SCTB (mg/cm2) | Left | 579.1 ± 76.5 | 588.7 ± 73.5 | 610.2 ± 45.4 | 590.0 ± 23.5 | 583.6 ± 71.5 | 596.9 ± 7.4 |
| Right | 562.7 ± 85.2 | 592.4 ± 64.4 | 632.8 ± 49.7‡ | 629.1 ± 28.3† | 575.5 ± 73.9 | 629.7 ± 20.4‡ | |
Spline is significantly (P ≤ 0.05) flatter than corresponding contralateral ROI.
See Table 2 for remainder of key.
In the frontal plane, SCBP density measurements for the left limb were significantly less than those for the right limb for the axial section and axial half section of the frontal midslice, caudal first slice, and caudal second slice (Table 2). Density measurements of SCTB in the left limb were significantly less than for the right limb for the axial section of the caudal first slice and the axial half section of the caudal second slice. In the sagittal plane, the left SCBP and SCTB density measurements were both significantly less than the right measurements for the caudal first section, caudal second section, and caudal half section of the axial slice.
Computed tomographic osteoabsorptiometry revealed that both SCBP and SCTB densities increased sequentially from the cranial second section to the caudal second section in the midsagittal plane (Figure 3 and 4). Exceptions to this pattern were identified at the axial section on the frontal midslice in the frontal plane and the cranial second section on the axial slice in the sagittal plane.
Density patterns as measured via CT osteoabsorptiometry in 5 frontal planes for SCBP (A) and SCTB (B) within 3 ROIs of MFCs from 6 Thoroughbred racehorse cadavers. Darkness of shading increases with increasing density as shown in panel C. The color scale denotes arbitrary density cutoffs and does not represent significant differences between individual ROIs. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Density patterns as measured via CT osteoabsorptiometry in 5 frontal planes for SCBP (A) and SCTB (B) within 3 ROIs of MFCs from 6 Thoroughbred racehorse cadavers. Darkness of shading increases with increasing density as shown in panel C. The color scale denotes arbitrary density cutoffs and does not represent significant differences between individual ROIs. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Density patterns as measured via CT osteoabsorptiometry in 5 frontal planes for SCBP (A) and SCTB (B) within 3 ROIs of MFCs from 6 Thoroughbred racehorse cadavers. Darkness of shading increases with increasing density as shown in panel C. The color scale denotes arbitrary density cutoffs and does not represent significant differences between individual ROIs. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Density patterns as measured via CT osteoabsorptiometry in 3 sagittal planes for SCBP (A) and SCTB (B) within 4 ROIs of MFCs from 6 Thoroughbred racehorse cadavers. See Figures 1 and 3 for remainder of key.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Density patterns as measured via CT osteoabsorptiometry in 3 sagittal planes for SCBP (A) and SCTB (B) within 4 ROIs of MFCs from 6 Thoroughbred racehorse cadavers. See Figures 1 and 3 for remainder of key.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Density patterns as measured via CT osteoabsorptiometry in 3 sagittal planes for SCBP (A) and SCTB (B) within 4 ROIs of MFCs from 6 Thoroughbred racehorse cadavers. See Figures 1 and 3 for remainder of key.
Citation: American Journal of Veterinary Research 74, 5; 10.2460/ajvr.74.5.691
Discussion
In the present study, no significant differences were found in width, length, or height between left and right MFCs from Thoroughbred racehorse cadavers. This finding supports results of a previous study22 in which gross measurements revealed no geometric asymmetry between left and right equine femurs distal to the femoral epicondyles; however, MFC curvature was not assessed in that study. We identified no differences between curvatures of left and right MFCs with the exception of 2 ROIs where the left spline was significantly greater (had less curvature) than the right MFC spline.
The left MFC had significantly greater spline than the right at the axial half section of the second cranial slice in the the frontal plane and the second caudal section in the midsagittal plane. Although significant, differences in radius were so minute that any clinical effect could be negligible. The 2 ROIs with significant spline variation were at different positions on the MFC, and no other differences in morphometrics between left and right MFCs were identified. When a value of P ≤ 0. 05 is used as a cutoff to indicate significance of statistical test results, one can expect 5% of results to be significant by chance. Because 43 spline measurements were analyzed, we would expect 2 ROIs to be significantly different by chance alone, which is equivalent to the obtained result. Given the minute differences between measurements and because they were identified at completely different ROIs in different planes, this variation can likely be attributed to the sensitivity of the spline measurement in our study or to chance.
Left and right stifle joints from 1 horse in the study had large full-thickness subchondral bone defects. Computed tomographic analysis revealed that both defects were a result of subchondral bone cysts. Both defects were located at the midsection of the cranial second slice in the frontal plane. There was a consistent flattening or concavity in the spline measurement at the midsection of the cranial second slice on 9 of 12 specimens. One horse had a bilateral concavity between the cranial second slice and cranial first slice that was not recorded because of the categorical nature of data collection. The small flattening or concavity on the cranial aspect of the MFC appeared to be at the same location as most subchondral bone cystic lesions in the MFC.
The most widely accepted theories for the pathogenesis of subchondral bone cystic lesions in horses include trauma and osteochondrosis.23 In 1963, Ondrouch24 first described the pathogenesis of bone cysts in humans as an overloading at uneven regions of a joint caused by osteoarthritis. Morphometric analysis of the cranial aspect of MFCs in the present study revealed a consistent concavity or flattening in the otherwise convex surface of the MFC. Each specimen had some degree of osteoarthritis present. This uneven region could have been caused by osteochondrosis or osteoarthritis or could have been an inherent characteristic of MFCs in horses. Furthermore, loading or trauma at this uneven articular surface could result in the development of subchondral bone cystic lesions24 caused by uneven loading and consequent bone remodeling. Although this uneven region was consistently identified in the MFCs of Thoroughbred racehorses in our study, more research needs to be performed to determine whether this uneven region is present in all horses of all sport disciplines and whether it is involved in the development of subchondral bone cysts.
Medial femoral condyle midsections in the frontal plane were generally the densest, compared with corresponding abaxial and axial ROIs, suggesting that most joint loading in Thoroughbred racehorses occurs midsagittally on the MFC. The SCBP and SCTB densities increased from the cranial second section to the caudal second section in the midsagittal plane. This finding supports that of another study18 in which caudally located osteochondral cores in the axial and midsagittal planes were denser than corresponding cranial cores in horses. A similar pattern exists in MFCs of dogs.19 In contrast to the other study18 in horses, the present study revealed densities of SCBP and SCTB that were consistently approximately 300 and 200 mg/mL denser, respectively, than the previously described osteochondral core densities. The reason for this discrepancy is likely that in the other study,18 cylindrical osteochondral core samples were used that were 5 mm deep with a 3.4-mm diameter. On the other hand, we analyzed pie-shaped ROIs that were widest at the CSC where the SCBP is most dense and came to an apex in the SCTB. Therefore, the previous findings were volume-averaged densities with proportionately more SCTB than the ROIs analyzed in our study. Furthermore, exact locations of the previously reported osteochondral core samples were not reported, so direct comparisons could not be made.18
An increase in density at the caudal aspect of MFCs in the midsagittal plane suggested that most joint loading occurs at that region.10 Furthermore, the caudal aspect of the MFC was the most common site of medial condylar arthrosis identified during gross examination. However, from examination of lateral stifle joint radiographs of standing horses, it is apparent that the cranial, rather than caudal, aspect of the MFC is loaded.25 Our results suggested that MFC loading in standing horses occurs cranioaxially on the MFC because cranial second sections at the axial aspect in both left and right limbs were consistently denser than the corresponding sections on midline or abaxially in the sagittal plane. Loading of the axial aspect of MFCs can also be seen on examination of the caudocranial radiographic projection in a standing horse.25
The increase in density in the caudal aspect of the MFC identified in other studies18,19 and in ours is due to dynamic biomechanical loading of the MFC. In a study26 of meniscal translocation and compression in horses, the cranial horn of the medial meniscus was found to undergo most compression between the cranial aspect of the MFC and the tibia, when the femorotibial joints were at full extension. Keeping these results in mind, one can infer that the caudalmost portions of the MFC undergo the greatest magnitude of loading when under flexion. Results from CT osteoabsorptiometry in the present study suggested that the caudal aspect of the MFC undergoes most of the concussion during locomotion. Although CT osteoabsorptiometry can provide tremendous insight into joint loading, a finite element analysis similar to one involving the distal equine third metacarpus of horses27 would be needed to determine the dynamic biomechanics of the medial aspect of the femorotibial joint.
Subchondral bone plate and SCTB densities at the axial section of the frontal midslice in frontal plane were consistently denser than corresponding axial sections on the other frontal slices (Figure 3). On examination of CT-generated 3-D models for 2 horses with intact stifle joints in extension, it was apparent that this is the region where the medial intercondylar eminence of the tibia comes into contact with the MFC. This finding suggested that the medial intercondylar eminence of the tibia affects the subchondral bone densities of the MFC and is actively involved in joint loading. It also supports a report by other investigators,28 who suggest that articulation of the medial intercondylar eminence of the tibia with the axial aspect of the MFC results in an outward rotation of the tibia.
No significant differences in subchondral bone density patterns between the left and right MFCs were identified in the present study except at the caudoaxial aspect of the MFC. All of the sections at this ROI were consistently denser in the right MFC than in the left for both SCBP and SCTB densities. A relevant flaw in the study design was that all racehorses were from the same North American racetrack, and 4 of 6 had been euthanized because of catastrophic forelimb injury. Asymmetries in hind limb subchondral bone density patterns could have been a result of compensation in gait because of forelimb lameness. Otherwise, discrepancies between left and right subchondral bone densities in the caudoaxial aspect of the MFC could have several potential explanations, including inherited or acquired conformational musculoskeletal asymmetries, preference in gait laterality, or repetitive asymmetric cyclic loading.
Although minimal, differences have been reported in geometry between the left and right long bones of horses.29 These differences are most profound in the metaphyseal region. Right metacarpal bones are longer than the left in racing Thoroughbreds and suggested to offer a competitive advantage when racing in a counterclockwise direction.30 Additionally, asymmetry between left and right femurs has been identified proximal to the MFC in Thoroughbred racehorses.22 Whether these discrepancies in geometry between left and right hind limbs are inherited or acquired has not been established, and it may be that differences in bilateral morphology elsewhere in the equine skeleton, such as the proximal femur, could result in asymmetric loading and subchondral bone density patterns in the MFC.
Laterality, also known as handedness, is the preferential usage of 1 side of the body. This phenomenon exists in mammals,31 reptiles,32 fish,33 birds,34 and amphibians.35 Laterality is a genetically linked trait believed to have developed early in vertebrate evolution.36 It has also been identified in horses37 and has been suggested to play a role in athletic performance.38 In Thoroughbred, Quarter Horse, and Arabian racehorses, 91% of trot-to-gallop transitions were found to be to the right lead, and 89% of horses galloping out of the starting gate start in the right lead.39 Breed or sex does not alter preference in laterality; when tested over 5 to 7 starts, horses started with the same stride pattern 94% of the time.39 Because of the consistency in limb preference among racing disciplines and between horses training and racing in a counterclockwise versus a clockwise direction, training and racing direction were not believed to influence laterality.39 It is possible that inherent gait preferences at the gallop and out of the starting gate influenced the MFC subchondral bone density patterns in the present study.
Repetitive asymmetric cyclic loading alters bone architecture in the metacarpal bones of racing Greyhounds because of adaptive remodeling40–42 and appears to influence the location and laterality of injuries in that population. Ninety-six percent of central tarsal bone fractures and 80% of accessory carpal bone fractures occur on the right side in racing Greyhounds,43,44 whereas 68% of metacarpal bone fractures involve the left side.45 Dissimilar to racing Greyhounds, Thoroughbred racehorses are not reported to have differences in cortical thickness between the left and right mid-diaphyseal region of the metacarpus46; however, several correlations have been made involving laterality and injury in Thoroughbred racehorses.
In the United States, 70% of completely displaced fractures of the metacarpal condyle occur on the right metacarpus,47 and 67% of forelimb fractures in the United Kingdom occur on the right side.48 Other studies in Thoroughbreds have revealed a higher incidence of third carpal bone fractures on the right versus left forelimb49 and proximal sesamoid bone injury on the left versus right forelimb.50 This association between laterality and incidence of injury has been suggested to be due to repetitive asymmetric cyclic loading, which is caused by counterclockwise racing in North America.47,51,52 In contrast, injury location and incidence are similar between Thoroughbreds racing in the United States and those racing in the United Kingdom, where Thoroughbreds race in counterclockwise and clockwise directions. This finding suggests that the incidence and laterality of racing injuries in Thoroughbreds may be due to inherent biomechanical factors rather than asymmetric cyclic loading.48
Nuclear scintigraphy has consistently revealed disparities in radiopharmaceutical uptake between the left and right hind limbs. Greater radiopharmaceutical uptake has been identified in right versus left stifle joints of a mixed equine population.53 This same pattern has been found in the sacroiliac,54 distal tarsal,55 and metatarsophalangeal joints56 of horses in the United Kingdom; however, the order in which images were acquired was not reported for any of these studies. If one supposes that the order at which images were acquired between left and right sides was random, then these findings suggest long-term asymmetric bone remodeling in horses.53
We hypothesize that the observed disparity between subchondral bone density patterns in left and right MFCs in Thoroughbred racehorses is attributable to the dynamic biomechanics of the stifle joint while undergoing asymmetric cyclic loading. In the United States, the right femorotibial joints of Thoroughbred racehorses undergo internal rotation during the cranial phase of motion to achieve propulsion in a counterclockwise direction, resulting in preferential loading of the right caudoaxial MFC on the medial intercondylar eminence of the tibia. External rotation would likely occur in the left femorotibial joint to achieve counterclockwise propulsion. To validate this hypothesis, femoral condyle osteoabsorptiometry and a finite element analysis of the stifle joint similar to the one performed for the distal aspect of the equine third metacarpus27 would need to be performed. The finite element analysis would need to be performed in a circular pattern rather than a straight line and at a gallop rather than a walk and trot and should also be performed in horses used in sport disciplines other than racing.
ABBREVIATIONS
| CSC | Cartilage-subchondral bone confluence |
| HU | Hounsfield unit |
| MFC | Medial femoral condyle |
| ROI | Region of interest |
| SCBP | Subchondral bone plate |
| SCTB | Subchondral trabecular bone |
Gemini TF Big Bore 16-slice scanner, Philips Medical Systems, Amsterdam, The Netherlands.
OsteoApp, Orthopaedic Research Center, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colo.
IDL, version 5.4, Research Systems Inc, Boulder, Colo.
Stata/SE, version 10.1, StataCorp LP, College Station, Tex.
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Appendix 1
Scale used for grading the gross appearance of cartilage in equine femurs.
| Cartilage grade | Description |
|---|---|
| 0 | Normal articular cartilage |
| 1 | Softening or discoloration |
| 2 | Partial-thickness defect |
| 3 | Full-thickness defect with normal subchondral bone |
| 4 | Full-thickness defect with erosion of subchondral bone |
Appendix 2
Scale used for grading the size of condylar surface lesions in equine stifle joints.
| Grade | Size (mm) |
|---|---|
| a | 0–4.9 |
| b | 5–14.9 |
| c | 15–24.9 |
| d | > 25 |