• View in gallery View in gallery

    Radiographic images (mediolateral views) of 2 cadaveric stifle joints collected from skeletally mature orthopedically normal Beagles in a study to investigate the effect of an excessive TPA on tensile forces experienced by the CCL, MCL, and LCL of canine stifle joints. A—Specimen from the unchanged TPA group. B—Specimen from the excessive TPA group after the TPA-increasing procedure was performed.

  • View in gallery

    Photograph (A) and schematic view (B) of the testing system used in the present study. A—The testing system consisted of a 6-DOF manipulator with a 6-DOF UFS. The upper and lower arrows indicate the tibial and femoral clamps, respectively. B—The 6-DOF robotic simulator was used to test the biomechanical behavior of the stifle joint, which has 3 translational (X, Y, and Z) and 3 rotational (U, V, and W) axes. The upper mechanism is indicated with a bracket on the right side of the image, and the lower mechanism is indicated with an arrow on the left side. The UFS (blue square in panel B) was used to measure load, moment, and torque and define the load applied to the joint. Horizontal and vertical straight dotted lines depict the X- and Z-axes, respectively, and the dotted circle depicts the site of the tibial clamp.

  • View in gallery

    Schematic depiction of the stifle joint coordinate system and controls in each direction. The 6-DOF stifle joint motions (blue arrows and double-headed arrows) along or around each axis (thick black lines) are shown. The stifle joint position was fixed, and flexion-extension rotation was maintained at 135° in the displacement control. Compressive loads of 30 and 60 N were each applied parallel to the tibial anatomic axis in the force control (in proximal-distal translation). Cranial-caudal and medial-lateral translation were controlled to maintain outputs in these directions at 0 N, and valgus-varus and internal-external rotation were controlled to maintain outputs in these directions at 0 Nm of force control; this prevented the generation of unnatural forces while the compressive load was applied in proximal-distal translation. The X-, Y-, and Z-axes of the femoral and tibial coordinate systems are shown in red and yellow, respectively (note that the X-, Y-, and Z-axes of the robotic system in Figure 2 are different from these axes). The conceptual drawing shows the motions of the femur and the tibia. CrCa = Cranial-caudal translation. FE = Flexion-extension rotation. IE = Internal-external rotation. ML = Medial-lateral translation. PD = Proximal-distal translation. VV = Varus-valgus rotation.

  • View in gallery

    Mean ± SD in situ tensile forces on the CrMB of the CCL, CaLB of the CCL, MCL, and LCL in cadaveric stifle joints of 8 skeletally mature Beagles of the unchanged TPA group at compressive loads of 30 N (white bars) and 60 N (gray bars). The force on each ligament was determined according to a previously described method.18 *Values are significantly (P < 0.05) different between the 30- and 60-N loads for a given ligament (paired t test). †Values are significantly different, compared with that for the MCL under the same load (ANOVA followed by the Tukey-Kramer test).

  • View in gallery

    Mean ± SD in situ tensile forces on the CrMB of the CCL, CaLB of the CCL, MCL, and LCL ligaments in cadaveric stifle joints of 8 skeletally mature Beagles of the excessive TPA group at compressive loads of 30 and 60 N. See Figure 4 for key.

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Investigation of the effects of excessive tibial plateau angle and changes in load on ligament tensile forces in the stifle joints of dogs

Tom Ichinohe BVSC, PhD1, Satoshi Yamakawa PhD1, Masakazu Shimada BVSC1, Nobuo Kanno BVSC, PhD1, Yukihiro Fujita BVSC, PhD1, Yasuji Harada BVSC, PhD1, Hiromichi Fujie PhD1, and Yasushi Hara BVSC, PhD1
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  • 1 From the Department of Small Animal Orthopedic Surgery, Veterinary Teaching Hospital and Laboratory of Small Animal Surgery, Azabu University, Kanagawa 252-5201, Japan (Ichinohe, Fujita); Biomechanics Laboratory, Faculty of System Design, Tokyo Metropolitan University, Tokyo 191-0065, Japan (Yamakawa, Fujie); and Laboratory of Veterinary Surgery, Nippon Veterinary and Life Science University, Tokyo 180-8602, Japan (Shimada, Kanno, Harada, Hara).

Abstract

OBJECTIVE

To investigate the effect of an excessive tibial plateau angle (TPA) and change in compressive load on tensile forces experienced by the cranial cruciate, medial collateral, and lateral collateral ligaments (CCL, MCL, and LCL, respectively) of canine stifle joints.

SAMPLE

16 cadaveric stifle joints from 16 orthopedically normal Beagles.

PROCEDURES

Stifle joints were categorized into unchanged (mean TPA, 30.4°) and excessive (mean TPA before and after modification, 31.2° and 41.1°, respectively) TPA groups. The excessive TPA group underwent a TPA-increasing procedure (curvilinear osteotomy of the proximal aspect of the tibia) to achieve the desired TPA. A robotic system was used to apply a 30- and 60-N compressive load to specimens. The craniomedial band of the CCL, caudolateral band of the CCL, MCL, and LCL were sequentially transected; load application was repeated after each transection. Orthogonal force components were measured in situ. Forces on ligaments were calculated after repeated output force measurements as the contribution of each component was eliminated.

RESULTS

Increasing the compressive load increased tensile forces on the craniomedial and caudolateral bands of the CCL, but not on the MCL or LCL, in specimens of both groups. At the 60-N load, tensile force on the craniomedial band, but not other ligaments, was greater for the excessive TPA group than for the unchanged TPA group.

CONCLUSIONS AND CLINICAL RELEVANCE

Results indicated that stress on the CCL may increase when the compressive load increases. The TPA-increasing procedure resulted in increased tensile force on the CCL at a 60-N compressive load without affecting forces on the MCL or LCL.

Abstract

OBJECTIVE

To investigate the effect of an excessive tibial plateau angle (TPA) and change in compressive load on tensile forces experienced by the cranial cruciate, medial collateral, and lateral collateral ligaments (CCL, MCL, and LCL, respectively) of canine stifle joints.

SAMPLE

16 cadaveric stifle joints from 16 orthopedically normal Beagles.

PROCEDURES

Stifle joints were categorized into unchanged (mean TPA, 30.4°) and excessive (mean TPA before and after modification, 31.2° and 41.1°, respectively) TPA groups. The excessive TPA group underwent a TPA-increasing procedure (curvilinear osteotomy of the proximal aspect of the tibia) to achieve the desired TPA. A robotic system was used to apply a 30- and 60-N compressive load to specimens. The craniomedial band of the CCL, caudolateral band of the CCL, MCL, and LCL were sequentially transected; load application was repeated after each transection. Orthogonal force components were measured in situ. Forces on ligaments were calculated after repeated output force measurements as the contribution of each component was eliminated.

RESULTS

Increasing the compressive load increased tensile forces on the craniomedial and caudolateral bands of the CCL, but not on the MCL or LCL, in specimens of both groups. At the 60-N load, tensile force on the craniomedial band, but not other ligaments, was greater for the excessive TPA group than for the unchanged TPA group.

CONCLUSIONS AND CLINICAL RELEVANCE

Results indicated that stress on the CCL may increase when the compressive load increases. The TPA-increasing procedure resulted in increased tensile force on the CCL at a 60-N compressive load without affecting forces on the MCL or LCL.

Introduction

Cranial cruciate ligament rupture is a common orthopedic disease of canine stifle joints.1 The CCL prevents cranial tibial displacement relative to the femur, excessive internal tibial rotation, and stifle joint hyperextension.2 Therefore, cranial tibial thrust, which is a primary force generated during weight-bearing on the hind limb,3 is not prevented in dogs with CCL rupture, and CCL rupture may cause an abnormal increase in internal stifle joint rotation. Dogs with CCL rupture may subsequently develop osteoarthritis and secondary meniscal damage of the affected joint.4 Although anterior cruciate ligament rupture can occur acutely as a result of trauma in people, most canine CCL ruptures are secondary to chronic degenerative changes in the CCL.5

In 1983, Slocum and Devine3 asserted that the tibial compression force directed cranially by the TPA causes CCL rupture. However, a study6 of 81 Labrador Retrievers found no difference in TPA between dogs with and without CCL rupture and no relationship between the magnitude of TPA and presence of CCL rupture. Currently, no consensus has been reached regarding this issue. One study7 found that dogs with CCL rupture and a TPA ≥ 35° (ie, excessive TPA) were younger than dogs with a TPA ≤ 30° (deemed a normal TPA). This finding suggests that dogs with an excessive TPA are at a higher risk of early CCL rupture than dogs with a TPA ≤ 30°.

In a previous study,8 our group showed that an excessive TPA (approx 40°) experimentally created by means of a TPA-increasing procedure may promote degenerative changes in the extracellular matrix of the CCL in dogs. However, not many studies have investigated the effects of excessive TPA on tensile forces experienced by the ligaments of canine stifle joints. The objective of the study reported here was to investigate the effects of excessive TPA on these forces by comparing the tensile forces on the CCL, MCL, and LCL in stifle joints from orthopedically normal Beagles with and without experimentally created excessive TPAs during in situ application of a compressive load selected to simulate weight-bearing conditions. A secondary aim was to compare the tensile forces on these ligaments between 2 loads (the estimate of weight-bearing force vs half of that force).

Materials and Methods

Specimen collection and preparation

Sixteen hind limbs with intact stifle joints were obtained from the cadavers of 16 skeletally mature Beagles that were euthanatized with an IV overdose of pentobarbital sodium solution for reasons unrelated to the present study. Euthanasia of the dogs was performed following the Guidelines for Care and Use of Laboratory Animals of Nippon Veterinary and Life Science University (approval Nos. 11-80 and 11-81). Radiographic and orthopedic screening confirmed that the intact stifle joints were free of osteoarthritis. The orthopedic screening included careful palpation to determine whether there was crepitus, a pain response during palpation, or an abnormal range of motion prior to euthanasia and gross visual observation during stifle joint arthrotomy. The specimens were arbitrarily divided into 2 groups of 8 specimens each: the unchanged TPA group and the excessive TPA group. The TPA of each specimen was measured on mediolateral radiographs by use of previously reported methods.9 The TPA of each selected stifle joint and the age, weight, and sex of the dog from which the specimen was obtained were recorded.

The femur of each specimen was transected at the hip joint, and the tibia and fibula were transected at the tarsocrural joint, as described in our previous study.10 The specimens were denuded of all soft tissue (excluding the joint capsules and ligaments), wrapped in gauze soaked in lactated Ringer solution, and stored at–20°C until used. The specimens were defrosted at 4°C overnight before experiments and were sprayed with lactated Ringer solution to prevent drying throughout the experimental procedures.10

TPA-increasing procedure

The TPA-increasing procedure was performed with a 30-mm TPLO saw bladea and a TPLO jig as described in another study8 performed by our group. The TPLO saw blade was used to change the shape of the proximal aspect of the tibia. The osteotomy was performed by centering the TPLO saw blade line on the midpoint between the medial and lateral intercondylar tubercles (the tibial functional axis remained unchanged). A 2.4-mm Kirschner wire, as a jig pin, was inserted 5 mm distal to the joint surface, caudal to the MCL, parallel to the articular surface and tibial coronal plane, and perpendicular to the patellar tendon. The jig was placed at the proximal jig pin, and a 2.4-mm Kirschner wire was placed through the distal jig pinhole on the jig arm and inserted parallel to the proximal jig pin. The saw blade was aligned parallel to the proximal jig pin and perpendicular to the tibial sagittal plane.9 To perform the osteotomy, the cranial blade edge was positioned perpendicular to the tibial crest, and the caudal edge was positioned perpendicular to the caudal aspect of the tibial cortex. The tibial plateau segment was rotated until the TPA was 40° after the osteotomy because the TPA may change after corrective osteotomy,11 although a TPA ≥ 34° is excessive.12 The amount of rotation (in millimeters) was calculated as 2 X 30(r) X ([40–TPA]/360)π, where r is the radius of the 30-mm TPLO saw blade.

A temporary increase in the TPA was achieved by inserting a 1.0-mm Kirschner wire across the osteotomy from the tibial crest to the tibial caudal cortex. The TPAs were modified by osteotomy of the proximal aspect of the tibia without changing the articular surface to minimize the effect of changes other than the TPA increase. Radiography was used to confirm that the TPA of the stabilized specimen was approximately 40°. The osteotomy was then stabilized with a 2.7-mm locking TPLO platea that was precontoured for anatomic fit, and the modified TPA was measured on mediolateral radiographs (Figure 1).

Figure 1
Figure 1
Figure 1

Radiographic images (mediolateral views) of 2 cadaveric stifle joints collected from skeletally mature orthopedically normal Beagles in a study to investigate the effect of an excessive TPA on tensile forces experienced by the CCL, MCL, and LCL of canine stifle joints. A—Specimen from the unchanged TPA group. B—Specimen from the excessive TPA group after the TPA-increasing procedure was performed.

Citation: American Journal of Veterinary Research 82, 6; 10.2460/ajvr.82.6.459

Tensile force testing

To enable clamp positioning for the testing system, the specimens were embedded in polymethyl methacrylateb at the proximal femoral and distal tibial margins.10 The robotic system used in the study was specifically developed to evaluate the biomechanics of the human knee joint and has been used for evaluation of canine stifle joint biomechanics in other studies.10,1315 The simulator used consisted of a 6-DOF manipulator with a 6-DOF UFSc (Figure 2), with simulation based on the knee joint coordinate system described by Grood and Suntay.16 The 6-DOF manipulator included 2 mechanisms (upper and lower). The upper mechanism could move in 2 translational and 3 rotational axes, and the lower mechanism could move in 1 translational axis. The tibial clamp was fixed to the upper mechanism via a UFS, and the femoral clamp was fixed to the lower mechanism.

Figure 2
Figure 2

Photograph (A) and schematic view (B) of the testing system used in the present study. A—The testing system consisted of a 6-DOF manipulator with a 6-DOF UFS. The upper and lower arrows indicate the tibial and femoral clamps, respectively. B—The 6-DOF robotic simulator was used to test the biomechanical behavior of the stifle joint, which has 3 translational (X, Y, and Z) and 3 rotational (U, V, and W) axes. The upper mechanism is indicated with a bracket on the right side of the image, and the lower mechanism is indicated with an arrow on the left side. The UFS (blue square in panel B) was used to measure load, moment, and torque and define the load applied to the joint. Horizontal and vertical straight dotted lines depict the X- and Z-axes, respectively, and the dotted circle depicts the site of the tibial clamp.

Citation: American Journal of Veterinary Research 82, 6; 10.2460/ajvr.82.6.459

The joint coordinate system was used to define the positions of the femur and tibia and motions of the joint in each stifle joint specimen. The motions that could be performed with the stifle joint were as follows: flexion-extension rotation, medial-lateral translation, valgus-varus rotation, cranial-caudal translation, internal-external rotation, and proximal-distal translation about each axis (Figure 3). The flexion-extension axis was defined on the basis of insertions of the MCL and LCL on the femur, and the internal-external rotation axis was defined on the basis of bone landmarks on the tibia. The valgus-varus axis was defined as the line perpendicular to the flexion-extension and internal-external rotation axes.

Figure 3
Figure 3

Schematic depiction of the stifle joint coordinate system and controls in each direction. The 6-DOF stifle joint motions (blue arrows and double-headed arrows) along or around each axis (thick black lines) are shown. The stifle joint position was fixed, and flexion-extension rotation was maintained at 135° in the displacement control. Compressive loads of 30 and 60 N were each applied parallel to the tibial anatomic axis in the force control (in proximal-distal translation). Cranial-caudal and medial-lateral translation were controlled to maintain outputs in these directions at 0 N, and valgus-varus and internal-external rotation were controlled to maintain outputs in these directions at 0 Nm of force control; this prevented the generation of unnatural forces while the compressive load was applied in proximal-distal translation. The X-, Y-, and Z-axes of the femoral and tibial coordinate systems are shown in red and yellow, respectively (note that the X-, Y-, and Z-axes of the robotic system in Figure 2 are different from these axes). The conceptual drawing shows the motions of the femur and the tibia. CrCa = Cranial-caudal translation. FE = Flexion-extension rotation. IE = Internal-external rotation. ML = Medial-lateral translation. PD = Proximal-distal translation. VV = Varus-valgus rotation.

Citation: American Journal of Veterinary Research 82, 6; 10.2460/ajvr.82.6.459

This system was selected for its ability to calculate the displacement and the force or moment applied to the knee or stifle joint, perform coordinate transformation of the data obtained by use of the UFS,17 and enable simulation of physiologic stifle joint motion controlled with respect to either the position (defined as the displacement control) or force (defined as the force control); it was also selected because it allowed the user to repeatedly replay the recorded motion.10 With this function, the system was capable of measuring joint laxity and also calculating the tensile force on ligaments according to the principle of superposition.18

The in situ force for each ligament was determined with a previously described method.18 The UFS recorded the output values of the 3 forces (fx, fy, and fz) during the application of mechanical motion and force for the joint just before transection of the targeted ligament. The ligament was then transected, the same motion and force were reapplied, and output values of the 3 forces (fx', fy', and fz') were recorded again. The in situ force on the intact ligament was calculated as the square root of ([fx – fx']2 + [fy – fy']2 + [fz – fz']2) as previously described.18

To simulate the condition of the stifle joint during weight bearing, compressive loads of both 30 and 60 N were applied to each mounted stifle joint in the proximal-distal direction (proximal-distal testing).14 Because the hind limb peak vertical force for normal dogs was reported to be equivalent to approximately 60% to 70% of body weight in a previous study,19 a 60-N compressive load (equivalent to approx 60% of the body weight of the cadavers in this study) was used. The procedure was also performed with half of this load (30 N) applied to observe the change in the in situ force experienced by each ligament with the change in load. The proximal-distal testing was performed and output recorded for each specimen under loads of 30 and 60 N as follows: first, with the joint and its ligaments intact; second, with the CrMB of the CCL transected; third, with the CaLB of the CCL transected; fourth, with the MCL transected; and last, with the LCL transected.

The system was initially set such that all UFS outputs were zero. The stifle joint was extended until a 0.5-Nm moment during flexion-extension rotation was applied in the force control; this condition was defined as the maximum extension. The joint angle at maximum extension was measured, and the tibial coordinate system was defined accordingly.10,14 To prevent the effect of tissue creep, the stifle joint was then extended and flexed 3 times from the maximum extension to a joint angle of 55° (the smallest joint angle attainable with the system used).10,14 The stifle joint position was then fixed with flexion maintained at 135° in the displacement control (midpoint of stance phase while walking),14 and the 30- and 60-N compressive loads were each applied parallel to the tibial anatomic axis in the force control of the proximal-distal translation.14 Medial-lateral and cranial-caudal translation were controlled to maintain outputs of these motions at 0 N, and the valgus-varus and internal-external rotation were controlled to maintain outputs at 0 Nm of force control, preventing the generation of unnatural forces during the proximal-distal translation testing (Figure 3). The outputs of the 3 forces in the UFS were recorded before (fx, fy, and fz) and after (fx', fy', and fz') transection of each ligament in the assigned order, and the in situ forces on each ligament were calculated as described.

For transection of the CrMB of the CCL, we performed joint incision and blunt dissection at the boundary line between the CrMB and CaLB orientation during sample preparation. Two nylon sutures were used as guides for transection; one was passed into the joint and around the CrMB, and the other was passed into the joint and around the entire CCL. After placement of these suture guides, the joint capsules were sutured closed. Transections were performed with a scalpel.

Statistical analysis

Data analysis was performed with statistical software.d The Shapiro-Wilk test confirmed that continuous data were normally distributed. The tensile forces on the CrMB of the CCL, CaLB of the CCL, MCL, and LCL were compared by means of 1-way ANOVA for repeated measurements, and the Tukey-Kramer test was performed for post hoc analysis. The paired t test was used to compare the TPA before and after osteotomy for the excessive TPA group and to compare the tensile forces on a given ligament type at compressive loads of 30 and 60 N. The 2-sample t test was used to compare the age, body weight, and TPA of dogs between groups prior to experimental procedures and to compare ligament tensile forces between the intact and excessive TPA groups at each load. Differences were considered significant at values of P < 0.05. These analyses were performed after the F test to evaluate homogeneity of variance. The results are reported as mean ± SD.

Results

The mean ± SD TPA of stifle joints was 30.4 ± 2.9° (range, 25° to 34°) and 31.2 ± 1.8° (range, 29° to 34°; prior to modification) for the unchanged and excessive TPA groups, respectively; these results did not differ significantly (P = 0.714) between groups. Similarly, the mean ± SD age (19.5 ± 12.2 months; range, 12 to 48 months) and body weight (9.5 ± 0.6 kg; range, 8.1 to 10 kg) for the unchanged TPA group did not differ significantly from those for the excessive TPA group (15.1 ± 2.4 months [range, 12 to 19 months; P = 0.348] and 10.4 ± 1.2 kg [range, 8.6 to 12.6 kg; P = 0.100], respectively). In the excessive TPA group, the mean ± SD TPA after osteotomy (41.1 ± 1.7°) was significantly (P < 0.001) greater than that prior to modification.

Tensile force testing

Unchanged TPA group

When the 30-N compressive load was applied, the in situ tensile forces on the CrMB of the CCL, CaLB of the CCL, MCL, and LCL in the unchanged TPA group were 8.0 ± 4.5 N, 8.4 ± 4.8 N, 2.8 ± 2.7 N, and 10.7 ± 11.4 N, respectively (Figure 4). No significant (P = 0.141) difference was found among the tensile forces on the 4 ligaments at this load. When the 60-N compressive load was applied, the tensile forces on the CrMB, CaLB, MCL, and LCL for this group were 10.7 ± 4.9 N, 15.6 ± 9.7 N, 2.9 ± 2.1 N, and 14.5 ± 7.8 N, respectively, with a significant (P = 0.003) difference among ligaments; post hoc testing indicated these forces on the CaLB and LCL were significantly (P = 0.004 and 0.010, respectively) higher than that on the MCL.

Figure 4
Figure 4

Mean ± SD in situ tensile forces on the CrMB of the CCL, CaLB of the CCL, MCL, and LCL in cadaveric stifle joints of 8 skeletally mature Beagles of the unchanged TPA group at compressive loads of 30 N (white bars) and 60 N (gray bars). The force on each ligament was determined according to a previously described method.18 *Values are significantly (P < 0.05) different between the 30- and 60-N loads for a given ligament (paired t test). †Values are significantly different, compared with that for the MCL under the same load (ANOVA followed by the Tukey-Kramer test).

Citation: American Journal of Veterinary Research 82, 6; 10.2460/ajvr.82.6.459

The in situ tensile forces on the CrMB and CaLB of the CCL in the unchanged TPA group were significantly (P = 0.007 and 0.010, respectively) higher at the 60-N compressive load than those at the 30-N load (Figure 4). In contrast, no significant difference in these forces was observed between the 30- and 60-N loads for the MCL (P = 0.844) or LCL (P = 0.210).

Excessive TPA group

When the 30-N compressive load was applied, the in situ tensile forces on the CrMB of the CCL, CaLB of the CCL, MCL, and LCL in the excessive TPA group were 7.7 ± 2.9 N, 10.0 ± 6.4 N, 1.2 ± 1.5 N, and 11.9 ± 9.5 N, respectively (Figure 5). Significant (P = 0.010) differences in these forces were detected among ligaments, and post hoc testing revealed that the tensile forces on the CaLB and LCL were significantly higher than that on the MCL (P = 0.030 and 0.007, respectively). At the 60-N compressive load, the tensile forces on the CrMB, CaLB, MCL, and LCL for this group were 16.4 ± 7.6 N, 20.8 ± 12.3 N, 1.2 ± 0.8 N, and 16.9 ± 11.0 N, respectively, with a significant (P < 0.001) difference among ligaments; on post hoc testing, these forces were significantly higher in the CrMB (P = 0.012), CaLB (P < 0.001), and LCL (P = 0.009) than in the MCL.

Figure 5
Figure 5

Mean ± SD in situ tensile forces on the CrMB of the CCL, CaLB of the CCL, MCL, and LCL ligaments in cadaveric stifle joints of 8 skeletally mature Beagles of the excessive TPA group at compressive loads of 30 and 60 N. See Figure 4 for key.

Citation: American Journal of Veterinary Research 82, 6; 10.2460/ajvr.82.6.459

The in situ tensile forces on the CrMB and CaLB of the CCL in the excessive TPA group were significantly (P = 0.002 and 0.002, respectively) higher at the 60-N compressive load than those at the 30-N load. However, no significant difference in these forces was found between the 30- and 60-N loads for the MCL (P = 0.939) or LCL (P = 0.189).

Intergroup comparisons

No significant difference was found between the unchanged TPA and excessive TPA groups for in situ tensile forces on the CrMB of the CCL (P = 0.894), CaLB of the CCL (P = 0.575), MCL (P = 0.174), or LCL (P = 0.823) when the 30-N compressive load was applied. At the 60-N compressive load, the tensile force on the CrMB was significantly higher in the excessive TPA group than in the unchanged TPA group, and the tensile force on the MCL was significantly lower in the excessive TPA group than in the unchanged TPA group (P = 0.004, 0.182, 0.020, and 0.311 for the CrMB, CaLB, MCL, and LCL, respectively).

Discussion

In a previous study,19 the hind limb peak vertical force in clinically normal dogs at a trot was reported to be approximately 60% to 70% of body weight. In the present study, because the typical force parallel to the tibial axis was unclear, we used a 60-N compressive load (equivalent to the lower value reported for peak vertical force; ie, 60% of the body weight of the dogs that specimens were collected from) to substitute for this force. Under this condition, the mean tensile forces on the CrMB and CaLB of the CCL were 10.7 and 15.6 N, respectively, in the unchanged TPA group. Thus, the mean tensile force on the CCL, accounting for the sum of the tensile forces in the 2 bands, was determined to be approximately 25 to 30 N (equivalent to approx 25% to 30% of the body weight of those dogs) in the unchanged stifle joints. Other investigators simulated the tensile forces on the CCL using a mathematical model of a structurally normal canine stifle joint with a TPA of 22° and reported that the maximum force during walking was 25% of body weight.20 Although the direction of the compressive loads differed between the present study (parallel to the tibial axis) and the previous study (perpendicular to the ground)20 and a direct comparison between the 2 studies was not possible, our results for the unchanged TPAs were fairly similar to those reported in that investigation.

In the present study, the increased compressive load resulted in increased in situ tensile forces on the CrMB and CaLB of the CCL in the unchanged and excessive TPA (defined for study purposes as approx 40°) groups. The tensile forces on the collateral ligaments did not change under this condition, suggesting that the focus of stress was on the CCL rather than on the collateral ligaments. Furthermore, a previous study3 found that body weight was greater in dogs with CCL rupture than in dogs without CCL rupture. These findings collectively suggest that as compressive force parallel to the tibial axis increases (eg, in obesity), stress on the CCL increases as well.

At the 60-N compressive load, the in situ force was generally higher in the CaLB than in the CrMB of the CCL, although the difference did not meet the criteria for significance. Results of another study2 reveal that the CaLB femoral and tibial attachments move closer to each other and the fibers relax as the stifle joint flexes in dogs; these attachments move apart, and the fibers grow taut as the joint extends. The CrMB conversely remains taut because the distance between the femoral and tibial CrMB attachments remains static during extension and flexion.2 These authors also suggested that the CrMB represents a smaller proportion of the CCL anatomy in comparison with the CaLB.2 For this reason, the CaLB may become taut at a stifle joint angle of 135°; therefore, the stress may be more focused on the CaLB than on the CrMB.

The CCL is responsible for maintaining craniocaudal stability in the stifle joint.1 An increase in TPA increases the cranial tibial shear force in the stifle joint and CCL stress.9 At the 30-N compressive load, tensile forces on the CaLB of the CCL and LCL were significantly higher than the force on the MCL in the excessive TPA group. In contrast, no significant differences in these forces were found between these ligaments and the MCL in the unchanged TPA group under the same compressive load. At the 60-N compressive load, tensile force on the CrMB was higher in the excessive TPA group than in the unchanged TPA group, suggesting that an increase in the cranial tibial shear force may increase CCL stress in stifle joints with excessive TPA as defined in this study. In a previous study21 of dogs with partial rupture of a CCL, the most commonly identified lesion was a rupture of the CrMB (20/25 dogs). Therefore, although results of the present study suggested that the tensile force on the CrMB is somewhat smaller than that on the CaLB (without a significant difference), our results indicated that as the TPA increases, a greater force that may lead to injury is generated on the CrMB.

Slocum and Slocum9 proposed that an increase in TPA may increase CCL stress and cause CCL rupture. In a study of dogs with CCL disease (rupture or partial rupture), Duerr et al7 reported that dogs with an excessive TPA (defined as ≥ 35°) were significantly younger at the onset of hind limb lameness than dogs with a TPA ≤ 30°, which suggests that dogs with an excessive TPA as defined in that study may have a greater risk of early CCL rupture than dogs with a TPA ≤ 30°. In our previous study,22 chondroid metaplasia and extracellular matrix alteration (changes similar to those in joints with a ruptured CCL) were observed in stifle joints in which the TPA was increased with the same previously described procedure8 used in the present study. In the present study, the data indicated that the tensile force on the CrMB of the CCL was significantly higher in the excessive TPA group than in the unchanged TPA group. This suggested that the proximal tibial shape may be important for the tensile forces experienced by the stifle joint ligaments and that an excessive TPA may magnify CCL stress and alter CCL strength, leading to a CCL rupture. On the basis of results of those previous investigations and the present study, and because dogs with an excessive TPA (≥ 35°) are at risk for sustaining a CCL rupture in the future, we suggest that these dogs should be monitored closely.

A limitation of the present study was that an in situ model lacking the musculature was used; therefore, an in vivo muscle force could not be reproduced and the effect of muscle force on the ligament tensile force could not be evaluated. In a previously described mathematical model of a structurally normal canine hind limb,20 the joint reaction force on the stifle joint ranged from 1.05 to 1.08 times the body weight, which was greater than the compressive load applied in the present study. Although previously mentioned differences prevented direct comparisons between results of the present study and that investigation,20 this suggested the compressive load used in our study may have been smaller than the forces experienced by canine stifle joints in vivo. It should also be noted that few dogs have a TPA of 40°. Moreover, it was possible that changing the order in which the ligaments were resected could have affected the tensile forces on ligaments. In particular, the CrMB and CaLB of the CCL were in contact with each other, and the tensile force on each ligament that was limited by this contact when the load was applied, such as during internal rotation, might have changed depending on the order of resection. Furthermore, although large dog breeds are more predisposed to CCL rupture than small breeds, our study was conducted with Beagles because this was the only breed available for research purposes in Japan. Only 1 joint angle (135°) was used because we anticipated that evaluations with different joint angles would be extremely time-consuming and would affect the mechanical characteristics of the tissues by deformation. The small sample size was also a notable limitation, but we could not obtain additional samples. Transecting and suturing the joint capsule could have had some effect on the results, although we tried to perform appositional suturing so that the in situ force generated in the joint capsule did not change. It was also possible that the attachments of the ligaments as well as proximal tibial shapes were changed by the TPA-increasing procedure in the excessive TPA group, which may have affected the results. Results of a previous study23 of dogs indicate that the angle between the tibial plateau and the patellar ligament is larger and the shear force on the CCL is greater in stifle joints with partial CCL rupture than in those with intact CCLs; these features could lead to overcharging of the CCL and contribute to the degenerative process in the CCL. Therefore, changes to the patellar ligament might influence the shear force on the CCL. Although the present study did not investigate the forces of the quadriceps muscle and patellar ligament, it was possible that translocation of the enthesis of the patellar ligament changed the shear force on the stifle joint.

The present study showed that tensile force on the CCL increased in situ with an increased compressive load while the collateral ligament tensile forces remained unchanged. We showed that an excessive TPA increases stress in the CCL, but not in the MCL and LCL. Moreover, the TPA-increasing procedure in this study increased the tensile force on the CCL without having a major impact on the MCL and LCL.

Acknowledgments

No funding was received in association with this study. The authors declare that there were no conflicts of interest.

The authors acknowledge Daichi Katori, Kotaro Kawakita, Yukino Suyama, Shoko Terashima, and Hitoshi Mukaitouge from Nippon Veterinary and Life Science University for their help with study experiments. English language editing was provided by Editage (www.editage.com).

Abbreviations

CaLB

Caudolateral band

CCL

Cranial cruciate ligament

CrMB

Craniomedial band

DOF

Degrees of freedom

LCL

Lateral collateral ligament

MCL

Medial collateral ligament

TPA

Tibial plateau angle

TPLO

Tibial plateau leveling osteotomy

UFS

Universal force-moment sensor

Footnotes

a.

Synthes Inc, West Chester, Pa.

b.

OSTRON2, GC Corp, Tokyo, Japan.

c.

UFS-IFS-40E 15A100-I63-EX, JR3 Inc, Woodland, Calif.

d.

BellCurve for Excel, version 3.21, Social Survey Research Information Co Ltd, Tokyo, Japan.

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Contributor Notes

Address correspondence to Dr. Ichinohe (ichinohe@azabu-u.ac.jp).