In vitro 3-dimensional kinematic evaluation of 2 corrective operations for cranial cruciate ligament-deficient stifle

Abstract

The objective of this study was to determine the immediate postoperative effect of 2 corrective operations for cranial cruciate ligament (CCL)-deficient stifle by evaluating 3-dimensional (3-D) stifle kinematics. Ten hindlimbs from large-breed canine cadavers were used. Range of motion was induced by applying 100 N of traction on the quadriceps tendon and recorded with electromagnetic movement sensors for each situation: intact stifle (control), CCL-sectioned stifle, and surgical correction of the sectioned ligament with the modified retinacular imbrication technique (MRIT) and then with a tibial plateau leveling osteotomy — Montavon (TPLO-M). The results for the experimental situations were compared with the results for the control situation by 1-way repeated-measures analysis of variance and with each other by post-hoc analysis with the least-significant-difference method. Range of motion was significantly decreased by MRIT as compared with the other situations. Normal cranial tibial translation was restored after MRIT, whereas TPLO-M resulted in significant caudal translation. A significant increase in external rotation was observed after both MRIT and TPLO-M. A significant increase in tibial adduction throughout the range of motion was observed with TPLO-M, whereas a significant increase in tibial abduction was observed after MRIT. This study allowed us to better understand objectively the effects on 3-D canine stifle kinematics of MRIT and TPLO-M. We suggest that this type of in vitro study would be useful to evaluate established and upcoming surgical techniques and potentially improve corrective surgery.

Introduction

Surgical options for repairing a ruptured cranial cruciate ligament (CCL) are numerous. During the last decade, a neutralizing dynamic technique, the tibial plateau leveling osteotomy (TPLO), has become as frequently used as the modified retinacular imbrication technique (MRIT) (1) as a result of articles suggesting that dogs undergoing TPLO have faster recovery, better function, and slower progression of osteophytosis (2–4). Recently, in a prospective study, Conzemius et al (5), using force plate analysis to compare outcomes, found no significant difference between dogs that had undergone lateral fabellar suture (LFS) or TPLO to correct CCL rupture: compared with clinically normal dogs only, 14.9% of the LFS-treated and 10.9% of the TPLO-treated dogs had normal limb function after surgery. In another study, Harper et al (6) confirmed the nonisometric position of traditional anchorage sites for the extra-articular reconstruction of CCL-deficient canine joints: using subjective observation of joint motion, they documented abnormal external rotation after surgery.

Subjective assessment (by the owner or by clinical evaluation) and objective assessment are used to determine the efficiency of the surgical technique in re-establishing stifle stability, full range of motion, and strength. Nevertheless, a lack of direct comparisons makes it difficult to draw conclusions (7,8). Currently, there is no consensus on the ideal surgical method for repairing a ruptured CCL (9).

Because it takes into account the complexity of the stifle, 3-dimensional (3-D) kinematic analysis is considered an objective method to assess surgical outcome in terms of joint motion (10). In vitro studies are of benefit because they enable direct comparison between surgical techniques performed on the same stifle. In addition, they are simple and less expensive than in vivo studies, and cadaver collection is easier than using live subjects. To our knowledge, no studies have reported the use of a 3-D kinematic device to evaluate the immediate effect of successive operations on canine stifle function.

The aim of our study was to document the immediate effects of MRIT and TPLO by performing a 3-D kinematic analysis on a simple and reproducible in vitro model. At the time of the study, TPLO — Slocum was patented, and for this reason we chose to use TPLO — Montavon (TPLO-M), which was developed to overcome the financial and legal constraints associated with the technique (11). We hypothesized that neither MRIT nor TPLO-M would re-establish normal 3-D kinematics in our model.

Materials and methods

Specimen selection and preparation

Ten hindlimbs (5 right, 5 left) from 8 adult large-breed dogs (1 rottweiller, 2 golden retrievers, 1 Labrador retriever, 1 Bernese mountain dog, and 3 mongrels) were used. All of the dogs had no history of ligament rupture or osteoarthritis. However, some had undergone previous surgery or had a diagnosis of a bone tumor on 1 of their hindlimbs, which explains the number of selected dogs compared with the number of evaluated limbs. The dogs were similar in size and body weight (range, 33 to 42 kg). Before the dogs were euthanized for reasons unrelated to this study, a clinical and radiographic stifle examination was performed by 2 independent examiners to exclude any abnormalities. The preoperative tibial plateau angle (TPA) was measured on digital radiographs as previously described (12). Our protocol was approved by the institutional animal care committee and followed the guidelines of the Canadian Council on Animal Care (13).

The hindlimbs were prepared for analysis by completely removing the muscles surrounding the femur and tibia. The periarticular tissues (joint capsule and retinaculum), collateral ligaments, and distal part of the quadriceps tendon (2 cm) were carefully preserved. Each specimen was placed in a saline-moistened towel, sealed in a plastic bag, and stored at −20°C until the day before testing; they were thawed at room temperature for 24 h before testing.

Testing apparatus and data collection

On the day of testing, the proximal end of the femur and the distal end of the tibia were transected at the level of the lesser trochanter and just proximal to the tibiotarsal joint, respectively. Then the extremities were fixed with polymethylmethacrylate (PMMA) (Impact-Plus; DenPlus, Longueuil, Quebec) in custom-made tubes with additional screw fixation to eliminate rotation at the PMMA–tube interface. The potted femoral end was mounted into the clamping cylinder of a custom-made testing apparatus, and the potted tibial end was guided into a vertical cylinder (Figures 1 and 2). A bearing mechanism allowed axial rotation as well as 3-D translations and could be locked.

Figure 1.

Schematic drawing of the testing device. ML — mediolateral; PD — posterodistal; AP — anteroposterior; IE — internal–external.

Figure 2.

Cadaver canine limb mounted in the testing device, with 3-dimensional (3-D) actuators fixed to the femur and tibia (arrows).

The stifle joint was positioned at the desired locked flexion angle by adjusting the orientation of the femoral clamping cylinder with respect to the fixed vertical orientation of the tibial cylinder. For each of the situations of intact stifle, CCL-sectioned stifle, and surgical correction with MRIT followed by TPLO-M on the same stifle, we recorded 3-D kinematics through 6 cycles of motion, from maximum flexion of the joint imposed by the apparatus to full extension. The extension motion was dynamically induced by applying a 100-N force on the quadriceps tendon with the use of calibrated pressure regulators, the tibial potted end having been removed from the tibial cylinder and the stifle being fixed only at the femoral end. Complete range of motion was divided into increments of 5° of flexion angle for statistical analysis. Results were obtained by coupling flexion and extension (the range of motion) with other motion axes. Only data for clinically relevant movements, such as internal and external rotation, adduction and abduction, and craniocaudal translation, were used for motion analysis.

During all tests, measurements were recorded at a registration rate of 60 Hz with a 3-D electromagnetic tracking system (Fastrack; Polhemus, Colchester, Vermont, USA). This allowed us to measure tibial motion relative to the femur. With the help of a digital pointer included in the measuring system, we developed a calibration process by using 3 points on the tibia and 3 on the femur to build a bone-embedded coordinate system that allowed the representation of movement, as described by Grood and Suntay (14). During the experiments, a saline mist was applied intermittently between each analysis to prevent tissue desiccation. One of the authors (N.C.) performed all the surgical procedures.

Unstable stifle

After initial testing of the intact stifle, the CCL was sectioned by means of a 2-cm lateral arthrotomy performed with a #12 scalpel blade under direct visualization. A Mosquito hemostatic clamp passed caudal to the CCL served as a guide, thus avoiding damage to the menisci and the caudal cruciate ligament. The presence of a cranial drawer motion in flexion and extension confirmed complete sectioning. The incision was then sutured with 3-0 polydioxanone (Ethicon, Johnson & Johnson Company, Somerville, New Jersey, USA) in a simple interrupted pattern, and the tibial end was repositioned in the tibial cylinder. Measurements were recorded as previously described.

First repair technique: MRIT

The MRIT technique was performed with the use of two 130-lb test nylon prostheses (Nylon, Special mer, Tortue La Soie-Neyme SAS, Boulogne, France) on the lateral side and 1 prosthesis on the medial side (15), tied manually by knots. Appropriate stabilization, defined as the absence of cranial drawer motion in flexion and extension, was verified manually by the surgeon. The tibia was freed from the cylinder during the procedure. The position of the hole within the tibial tuberosity was standardized according to anatomic landmarks, as previously described (16). The distance between the proximal and distal parts of the insertion of the patellar tendon defined 1 side of the triangle. The 2nd side was drawn perpendicular to the 1st side. The hole was created at the intersection of the 3rd side and the 2nd side for each specimen. Once the prostheses were in place, the tibial end was repositioned in the tibial cylinder, and measurements were recorded as previously described.

Second repair technique: TPLO-M

After the nylon prostheses were removed, TPLO-M was performed on the same stifle. A proximal tibial wedge ostectomy was performed as described by Damur et al (11). The lateral and medial arthrotomies were closed with 3-0 polydioxanone sutures in an appositional cruciate pattern. The TPA was not directly measured postoperatively. Instead, a 15° template consisting of a #11 blade tip was used as a landmark of the tibial wedge; the postoperative TPA was obtained by subtracting 15° from the initial TPA. The tibial end was replaced in its cylinder, and measurements were recorded as previously described.

Statistical analysis

One specimen was discarded because of an error in the axes’ definition at the beginning of the experiment. Therefore, data for 9 stifles were statistically analyzed. First, a 1-way analysis of variance for repeated measures was performed to compare the data for the 4 situations. If a statistically significant difference was found, we did a post-hoc analysis to compare the means for pairs of situations. A P-value of less than 0.05 was considered significant.

Results

The average preoperative TPA was 26.22° (standard deviation, 2.6°; range, 23° to 30°) and the average postoperative TPA 11.22° (standard deviation, 2.6°; range, 8° to 15°) (Table I). The range of motion was analyzed between 95° and 30° of flexion. Towards full extension, oscillation of the tibia led to unreliable values.

Table I.

Tibial plateau angle (TPA) before and after tibial wedge ostectomy of 15° and postoperative tibial translation values for 9 canine hindlimbs

	TPA (°)
Stifle no.	Preoperative	Postoperativea	Average tibial translation(mm)
1	26	11	−9.15
2	24	9	−12.17
3	23	8	−19.48
4	26	11	−11.39
5	30	15	−4.23
6	25	10	−7.34
7	24	9	−11.60
8	30	15	−5.50
9	28	13	−5.82

^aCalculated as the preoperative value minus 15°; the postoperative angle could not be measured because of the absence of the tarsal joint, resected for the experiment.

After CCL section, the range of motion was unchanged. Cranial displacement was observed from 45° to 30° of flexion, but it was not significant when compared with the normal stifle (Figure 3). The tibial rotation did not significantly change (Figure 4). In adduction and abduction, no significant difference was observed (Figure 5).

Figure 3.

Comparison of the tibial translation of the passive stifle movement in each experimental situation: intact stifle (horizontal line), sectioned cranial cruciate ligament (CCL) (hatched bars), sectioned ligament repaired with the modified retinacular imbrication technique (MRIT) (black bars), and further repair by means of tibial plateau leveling osteotomy — Montavon (TPLO-M) (grey bars). The stars indicate significant differences as compared with the intact stifle, and the daggers represent significant differences as compared with the CCL-sectioned stifle.

Figure 4.

Comparison of the tibial rotation of the passive stifle movement in each situation. Bars and symbols as in Figure 3.

Figure 5.

Comparison of the tibial abduction and adduction of the passive stifle movement in each situation. Bars and symbols as in Figure 3.

After MRIT, the range of motion was significantly decreased from 60° to 35° of flexion compared with both normal and CCL-sectioned stifle. The MRIT did not create cranial displacement (Figure 3) but did increase external rotation and abduction over the decreased range of motion (Figures 4 and 5).

After TPLO-M, the range of motion was unchanged. We observed significant caudal translation (Figure 3) during the range of motion that decreased significantly at a postoperative TPA of more than 11° (Table I). External rotation was significantly increased from 90° to 30° of flexion (Figure 4), and there was a significant increase in tibial adduction that increased with flexion (Figure 5).

Discussion

Stifle motion has been described in various ways in the literature. The recent development of computer-assisted techniques to evaluate surgical procedures, CCL repair in particular, provides new methods of evaluating and potentially improving stifle kinematics that should also improve functional outcome. Studies have established that only passive tests that investigate rotational and craniocaudal stability can discriminate the CCL status and the objective effects of corrective surgery (4). Three-dimensional kinematic evaluation of the joint has the advantage of accurately measuring 6 independent parameters and describing them in a comprehensible manner. In fact, the stifle is a complex structure capable of sliding and rolling, combining 3 rotations and 3 translations. To our knowledge, no study has assessed the effect of cranial ligament reconstruction on 3-D kinematics during continuous movement. The proposed evaluation method allows us to quantify the kinematics along different axes of rotation (craniocaudal translation, tibial rotation, and abduction). As demonstrated previously, the electromagnetic device is accurate, repeatable, and reliable for in vitro studies, with precision of ± 0.5 mm in translation and ± 1° in rotation (17). Moreover, by using the same system of reference axes in all situations for a given stifle, we eliminated the problems associated with defining anatomic rotational axes. That allowed us to use the intact stifle as its own control, which enabled us to compare data among the limbs used in this study. The methods and technical choices were based on a method developed for a study in humans (10). An analysis of stifle motion was performed in complete free motion except for quadriceps traction to create the motion. In the normal stifle, tibial internal rotation occurs naturally during joint flexion, to slowly tend toward external rotation in almost complete extension. Motion limitations are in part controlled by ligamentous constraints and condylar geometry (18). Our in vitro study approximated events during the gait cycle’s non-weight-bearing phase, as a slow walk stride taken after the swing phase and before the stance phase. In that situation, the limb is never in complete extension. In free-motion conditions, such as with our kinematic model, the isolated CCL section amplified motions of the intact stifle without making them significantly greater. A weight-bearing simulation would likely have created a greater cranial tibial thrust.

In the absence of the CCL, one can presume that quadriceps contraction will cause cranial tibial subluxation at flexion angles ranging from 0° to 45°. Our valid registration range of motion stopped at 30° of flexion. Even if quadriceps contraction may be a component driving the cranial tibial subluxation, it does not seem to be the main force creating a significant cranial translation. Moreover, in vivo studies have shown that cranial drawer motion is especially marked toward complete extension, at the stance phase (19).

The 1st surgical procedure, MRIT, significantly altered the range of motion in our cadaver model in free motion. This restriction is a direct consequence of the nonisometric placement of the prostheses, as described by Harper et al (6). Moreover, we observed that MRIT not only limited cranial displacement in the unloaded cadaver stifle but also created constant external rotation and abduction along the limited range of motion. This was likely due to the placement of the lateral prosthesis. Therefore, the role of the medial prosthesis is questionable. Further comparative testing of MRIT with or without a medial prosthesis is necessary. As well, excessive external rotation with constant abduction may induce excessive lateral tibial- compartment compression. The analyses were done immediately after the surgical procedure. Further studies done on a weight- bearing cadaver model and under cycling conditions would be useful to determine if this compression would persist and for how long. If so, the tension of the sutures and anchor points might be the subject of further studies so that they could be adjusted.

With TPLO-M, using a standard 15° ostectomy wedge, each specimen had a postoperative TPA above 6.5°, the final recommended angle (20). At postoperative TPAs above 6.5°, tibial plateau leveling was still effective in reversing the cranial tibial thrust in a caudal tibial thrust (19). At a higher postoperative TPA, caudal tibial translation was significantly less important. Thus, it might not be necessary to obtain a postoperative TPA as close as the previously recommended 6.5°. It would be important to support these findings with a weight-bearing model.

With the use of TPLO-M, passive range of motion was preserved throughout the range evaluated, 95° to 30° of flexion. Our data on internal and external rotation and adduction and abduction were completely different from those for TPLO — Slocum in the veterinary literature (12). Instead of internal rotation associated with abduction, we observed external rotation combined with adduction. Because TPLO is a dynamic neutralizing technique, we should have found results similar to those for CCL-sectioned stifle except when tibial ostectomy modified the proximal tibial anatomy with the femur. According to a recent TPLO — Slocum study, the accuracy of the osteotomy has an impact on the angular deviation and the rotation of the tibia (21). In our study, landmarks for the ostectomy were placed on the medial tibial cortex, as recommended by Damur et al (11). The cut of the proximal tibia created a varus and allowed external rotation throughout the range of motion. According to these results, correction of tibial deformity using the technique should be taken into account at the end of the procedure.

We are aware of the limitations of our study. First, the fact that it was an in vitro study limits the conclusion as to the immediate effect of CCL reconstructions. Especially in the case of MRIT, it can be hypothesized that the suture will loosen over time, and joint stability and kinematics will then change. Second, the model simulates a non-weight-bearing situation. Therefore, our conclusions were limited to the swing phase of a dog’s walk. In addition, removal of all muscles but the quadriceps force greatly simplifies the model and renders comparison with the clinical setting difficult. The complexity of the stifle makes it hard to create an assembly that implements all the forces influencing articular mobility. However, despite its relative simplicity, this in vitro model has the advantage of keeping the intact stifle as its own control, thus preserving the same experimental conditions for each limb. Also, our objective results support previous subjective data. Finally, it must be noted that this was an initial attempt to document 3-D movement of the stifle in order to improve our understanding of the immediate effects of surgery.

The results of this study demonstrate that even if craniocaudal laxity is restored with MRIT (as verified manually by the surgeon), this reconstruction affects the range of motion and tibial rotation immediately after surgery, at least in this model. That may translate into nonphysiologic forces in vivo. Moreover, a modification of tibial rotation was observed after TPLO-M. Therefore, one might ask whether reconstruction should aim only at restoring stifle laxity or whether attention should be paid to restoring 3-D stifle kinematics. With the improvement of devices, in vitro studies simulating weight-bearing and further in vivo studies could become a useful additional step to corroborate and complete our findings.