Introduction
The function of the cranial cruciate ligament (CCL) is to restrict cranial displacement of the tibia in relation to the femur, to limit internal tibial rotation during flexion, to counteract joint hyperextension, and to ensure the stability of the varus and valgus motion of the stifle joint.1 CCL rupture is among the most common orthopedic injuries in dogs, and it is the main cause of pelvic limb lameness in these patients.2 The etiopathogenesis of ligament insufficiency or rupture can be traumatic, but in most cases, it is degenerative, and anatomical factors, including the tibial plateau angle and bone rotational deviations, are related to the condition.3 CCL rupture causes joint instability and changes the biomechanical mechanism of the stifle due to cranial tibial translation, which triggers progressive osteoarthritis.4
In dogs, CCL rupture is most commonly diagnosed by means of specific orthopedic tests, such as the drawer test and the tibial compression (TC) test, both of which assess joint stability and promote cranial tibial translation in relation to the femur if ligament insufficiency or rupture is present.5 Complementary imaging-based tests may prove helpful for diagnosis and are, in general, useful in preoperative planning, the evaluation of osteoarthritis, and the identification of concomitant affections.6 Cranial tibial translation detected by radiography is indicative of CCL rupture; however, it must be interpreted in association with clinical findings. Radiography performed under joint stress by means of TC might be more accurate in indicating CCL insufficiency or rupture.3,7 In mediolateral radiographic projections of the stifle, conventional joint positioning and positioning under TC are strong indicators in the diagnosis of CCL rupture, which can also be used to assess the efficacy of treatment.3
The aim of this study was to assess the specific quantitative parameters of cranial tibial translation that allow for a radiographic diagnosis of CCL rupture in dogs. A comparative analysis was conducted to assess the effect of TC in radiographs of the stifles of healthy adult dogs, adult dogs with CCL rupture, and healthy young dogs. The hypothesis was that dogs with ligament rupture exhibit significantly different values compared with those for healthy dogs in the analyses of radiographic images taken under TC. Furthermore, a novel variable was proposed for the quantitative diagnosis of rupture: the ratio of the distance between the points of CCL origin and insertion, obtained from radiographs taken under TC and without TC.
Materials and Methods
The present study was submitted to the Ethics Committee on Animal Use of the Federal University of Lavras, and approval was granted under protocol No. 052/2017.
The study was conducted in the facilities of the University Veterinary Hospital, and it was divided into 2 phases of dog selection. In the first phase, a retrospective study of radiographic images of dogs with a surgical diagnosis of complete unilateral CCL rupture was undertaken. In the second phase, a prospective study with selection of young and adult dogs without CCL rupture was performed.
Initially, the inclusion criteria for the study of dogs with CCL rupture were determined and comprised radiographs taken under no sedation or anesthesia and with adequate positioning, the absence of other musculoskeletal injuries, and body weight between 15 and 40 kg, taking into consideration the epidemiology of the disorder according to one previous study,3 irrespective of sex, breed, or etiology of the ligament rupture. The following radiographic positioning criteria were established: mediolateral projections of the affected pelvic limb with the radiographic beam centered over the stifle and presence of a conventional radiograph with no TC (NTC) and a radiograph taken under joint stress by means of TC, with visibility of the talus bone to delineate the tibial mechanical axis, overlapping femoral condyles with a maximum gap of 2 mm between their borders, and a 135 ± 5° stifle joint angle. In both projections, to obtain the radiographic image with the stifle joint positioned at approximately 135°, the joint was correctly angled with the aid of a goniometer, which allowed the uniformity of stifle joint position. In the TC radiographs, while the stifle joint was maintained in the proper position, the tibiotarsal joint was flexed to 90° to promote cranial translation of the tibia.
In the retrospective phase, a search was carried out of all medical records of patients operated on in the service with complete unilateral rupture of the CCL between 2015 and 2018. The search subsequently excluded data from dogs that did not fit the clinical and radiographic inclusion criteria. The remaining medical records and surgical files were carefully analyzed, excluding those in which there was a description of exacerbated medial buttress, advanced osteoarthritis, and partial rupture of the CCL. Initially, the radiographs of 32 dogs with the condition were selected, but 12 dogs were still excluded. Of these, 9 dogs did not have adequate overlapping of the femoral condyles, and 3 dogs had clinical records of previous stifle joint surgery. Meniscal injury seen at surgery was not an exclusion factor. Therefore, radiographs of 20 dogs could finally be included in the study, corresponding to the group of adult dogs with CCL rupture.
In the second phase of the study, the selection and radiographic examination of 20 healthy adult dogs and 20 healthy young dogs were undertaken prospectively. Dogs were determined to be healthy after orthopedic and radiographic examination by an experienced professional, and those exhibiting any type of musculoskeletal disorder were excluded. The inclusion criteria for the group of healthy adult dogs were a body weight between 15 and 40 kg and an age between 18 months and 6 years. Healthy young dogs were aged between 6 and 10 months, with a body weight > 15 kg. Selection was not based on sex or breed. One pelvic limb per healthy dog was randomly selected and radiographed, and no type of sedation or anesthesia was used. The radiographic positioning criteria applied were the same as those used in the group of dogs with CCL rupture, and mediolateral radiographs were also taken in 2 projections: NTC and TC.
Radiographs of 60 dogs were included for the study and divided into 3 groups with 20 dogs each: group 1 (G1), healthy adult dogs; group 2 (G2), adult dogs with CCL rupture; and group 3 (G3), healthy young dogs. Radiograph measurements were conducted by 2 experienced radiographic interpreters blinded to the animal groups. After proper acquisition of each variable, it was measured 3 times at different time points, and the mean of each variable was used for statistical analysis.
The patellar ligament angle was measured in relation to the common tangent at the tibiofemoral contact point (Figure 1). The patellar ligament insertion angle was measured following the recommendations of a previous study on tibial cranial angles8 (Figure 2). The angle of tibial translation a (ATTa) was measured according to a method established in a 2017 study.9 The authors of the present work proposed a modification to this assessment. Specifically, the site of measurement was changed, and a new angle was found. Thus, ATTa stands for the angle obtained by the method already described in the literature, whereas angle of tibial translation b (ATTb) indicates the modified method (Figure 3).

Radiographic image (mediolateral projection) of the stifle joint of a dog, showing the patellar ligament angle (PLA).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528

Radiographic image (mediolateral projection) of the stifle joint of a dog, showing the patellar ligament angle (PLA).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528
Radiographic image (mediolateral projection) of the stifle joint of a dog, showing the patellar ligament angle (PLA).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528

Radiographic image (mediolateral projection) of the stifle joint of a dog, showing the patellar ligament insertion angle (PLIA).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528

Radiographic image (mediolateral projection) of the stifle joint of a dog, showing the patellar ligament insertion angle (PLIA).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528
Radiographic image (mediolateral projection) of the stifle joint of a dog, showing the patellar ligament insertion angle (PLIA).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528

Radiographic image (mediolateral projection) of the pelvic limb of a dog, showing angle of tibial translation a (ATTa) and angle of tibial translation b (ATTb).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528

Radiographic image (mediolateral projection) of the pelvic limb of a dog, showing angle of tibial translation a (ATTa) and angle of tibial translation b (ATTb).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528
Radiographic image (mediolateral projection) of the pelvic limb of a dog, showing angle of tibial translation a (ATTa) and angle of tibial translation b (ATTb).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528
Additionally, cranial tibial displacement in relation to the femur was measured according to the method proposed by the authors of a previous study.3 Conventional mediolateral radiographic images and those taken under TC were used to measure the distance between the point of origin of the CCL in the femur and the point of CCL insertion in the tibia (DPOI; Figure 4). In terms of radiography, the site considered as the CCL origin in the femur was localized at a point adjacent to the distal aspect of the lateral fabella on the caudal border of the proximal femoral condyle (caudal-proximal point of the Blumensaat line). The site of CCL insertion in the tibia was located at the cranial border of the medial tibial condyle. Considering the variations in weight and anatomical conformations and because this is a linear measure, the authors of the present work proposed a ratio dividing the DPOI value obtained from the radiograph under TC by the DPOI value from the conventional radiograph, thus generating the new variable DPOI ratio to eliminate the bias caused by dog variation.

Radiographic images (mediolateral projection) of the stifle joint of a dog, taken under conventional positioning with no tibial compression (NTC) and with tibial compression (TC), showing the distance between the origin and insertion (red line) of the cranial cruciate ligament. When comparing both positioning methods, note that this animal had tibial displacement of 5.6 mm.
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528

Radiographic images (mediolateral projection) of the stifle joint of a dog, taken under conventional positioning with no tibial compression (NTC) and with tibial compression (TC), showing the distance between the origin and insertion (red line) of the cranial cruciate ligament. When comparing both positioning methods, note that this animal had tibial displacement of 5.6 mm.
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528
Radiographic images (mediolateral projection) of the stifle joint of a dog, taken under conventional positioning with no tibial compression (NTC) and with tibial compression (TC), showing the distance between the origin and insertion (red line) of the cranial cruciate ligament. When comparing both positioning methods, note that this animal had tibial displacement of 5.6 mm.
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528
All the obtained data were tested for normality (Shapiro-Wilk test) and homogeneity (Bartlett test). Parametric variables were assessed with ANOVA, and differences in the comparison of data from each variable were considered significant at P < .05. The effect of radiography performed under TC was tested in all assessed variables within each group with the paired t test. Subsequently, each variable (except for DPOI ratio) was tested for differences (Tukey multiple comparison test) with and without TC on radiography among the 3 dog groups. The DPOI radio was not normally distributed, and the Kruskal-Wallis and Mann-Whitney tests were chosen to assess significant differences between groups. To improve the analyses, each variable was identified according to radiographic positioning (ie, either conventional radiography NTC or under joint stress with TC). Intraclass correlation coefficient and CI of each variable were used for interobserver analysis. Statistical analyses were performed, and to predict the diagnostic value of DPOI ratio, regression analysis was conducted with a receiver operating characteristic (ROC) curve to establish a diagnostic cutoff point for this variable.
Results
Mean and SD were calculated for all variables. In G1 (healthy adult dogs), images from 13 males and 7 females with a mean body weight of 33 kg (SD ± 4.6 kg) and a mean age of 4 years (SD ± 2.8 years) were selected. In G2 (CCL ruptured dogs), images were taken of dogs with a mean body weight of 37 kg (SD ± 7.1 kg) and a mean age of 6 years (SD ± 3.2 years), among which 12 were females and 8 were males. In G3 (healthy young dogs), radiographic images of 11 females and 9 males, with a mean age of 7 months (SD ± 1.8 months) and a mean body weight of 29 kg (SD ± 3.5 kg), were taken. Considering all groups, 50% of the dogs were male, and 50% were female.
Statistical significance of radiographic measurements obtained under TC was found among most variables within groups, except for the DPOI in G1. This result showed that DPOI could achieve higher precision in differentiating dogs without CCL rupture when measured under TC because joint stress did not interfere with the results of these variables within G1 due to ligament integrity. Regarding the DPOI values under TC, the mean for the G3, both regarding the linear measurement for DPOI and the DPOI ratio, was between those for G1 and G2 (G1 < G3 < G2). Thus, the evaluation of DPOI showed that TC promoted minimal cranial tibial displacement in healthy adult dogs, moderate displacement in healthy young dogs, and pronounced displacement in dogs with CCL rupture.
The results of the comparative analysis among the 3 groups are shown (Figure 5). In the comparative analysis among the 3 groups regarding patellar ligament angle, there was no difference among them using TC. With NTC, there was no difference among the groups for patellar ligament angle, patellar ligament insertion angle, and DPOI, which showed no significant difference between the groups.

Graphs of the comparative analysis between the groups with values obtained from radiographic images taken with NTC or with TC in healthy adult dogs (G1), dogs with cranial cruciate ligament rupture (G2), and healthy young dogs (G3). [A]—PLA. [B]—PLIA. [C]—ATTa. [D]—ATTb. [E]—Distance between the origin and insertion (DPOI) of the cranial cruciate ligament. Above the bars, different letters mean statistical difference among groups. *Statistically significant at P < .05.
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528

Graphs of the comparative analysis between the groups with values obtained from radiographic images taken with NTC or with TC in healthy adult dogs (G1), dogs with cranial cruciate ligament rupture (G2), and healthy young dogs (G3). [A]—PLA. [B]—PLIA. [C]—ATTa. [D]—ATTb. [E]—Distance between the origin and insertion (DPOI) of the cranial cruciate ligament. Above the bars, different letters mean statistical difference among groups. *Statistically significant at P < .05.
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528
Graphs of the comparative analysis between the groups with values obtained from radiographic images taken with NTC or with TC in healthy adult dogs (G1), dogs with cranial cruciate ligament rupture (G2), and healthy young dogs (G3). [A]—PLA. [B]—PLIA. [C]—ATTa. [D]—ATTb. [E]—Distance between the origin and insertion (DPOI) of the cranial cruciate ligament. Above the bars, different letters mean statistical difference among groups. *Statistically significant at P < .05.
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528
The ATTa values obtained without TC were significantly different among the groups (P = .002), and the same occurred for this variable in radiographs with TC, in which the 3 groups exhibited significant differences among each other (P < .0001). Comparative analysis of ATTb revealed statistical results similar to those obtained for ATTa (ie, all groups exhibited statistically significant differences from each other in both radiographic positions, with and without TC).
By the Tukey test, DPOI without TC was considered nonsignificant between the groups. The comparison of this variable between groups under TC showed significance, with P values < .0001. The mean distance, in millimeters, was higher in dogs with CCL rupture (G2), and the greatest value difference was found between healthy adult dogs (G1) and those with CCL rupture (G2). The pronounced cranial tibial translation in dogs with CCL rupture increases in a linear manner with increasing DPOI.
The analysis of DPOI ratio revealed significant differences among all the groups (P < .0001). For this variable, an ROC curve predictive analysis indicated 100% specificity and 99.9% sensitivity for this ratio in the comparison of the healthy dogs with dogs with CCL rupture. An accuracy of 1.0 for a DPOI ratio > 1.18, with no interpolation of results whatsoever between dogs in G1 and in G2, was obtained. In the ROC curve analysis, a cutoff point to differentiate G3 from G1, with 100% of specificity and 85% of sensitivity, was 1.05. In radiographic imaging, young dogs should be differentiated by assessing an intermediate DPOI ratio value together with other factors, such as the detection of open epiphyseal plates in radiographic images and signs of degenerative joint disease. The results showed that G3 always exhibits intermediate values, with a trend toward similarity with G1 in cumulative frequency analysis.
The results obtained with the diagnostic test showed that DPOI ratio has high potential as a CCL rupture diagnostic measure, given that it exhibited high specificity and sensitivity, with better differentiation of healthy dogs. In the present study, DPOI ratio values above 1.18 were sufficient to accurately confirm the diagnosis of CCL rupture, completely differentiating dogs in G2 from healthy adult and young dogs (G1 and G3) (Figure 6).

Multiple comparison analysis graph of the variable DPOI ratio in healthy adult dogs (G1), dogs with cranial cruciate ligament rupture (G2), and healthy young dogs (G3).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528

Multiple comparison analysis graph of the variable DPOI ratio in healthy adult dogs (G1), dogs with cranial cruciate ligament rupture (G2), and healthy young dogs (G3).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528
Multiple comparison analysis graph of the variable DPOI ratio in healthy adult dogs (G1), dogs with cranial cruciate ligament rupture (G2), and healthy young dogs (G3).
Citation: Journal of the American Veterinary Medical Association 261, 10; 10.2460/javma.22.11.0528
For interobserver analysis, an intraclass correlation (ICC) above 0.75 was considered excellent, between 0.4 and 0.75 was considered satisfactory, and below 0.4 was considered poor. The results of this analysis showed that more complex measurements with a higher number of anatomical reference points were the most susceptible to variation when assessed by different professionals. Patellar ligament insertion angle and ATTa showed ICC of 0.32 and 0.25, respectively. The patellar ligament angle (ICC = 0.72), ATTb (ICC = 0.70), and DPOI (ICC = 0.88) showed values that indicate a high correlation between the measurements performed by different evaluators. These data showed that it is better to choose simpler but equally efficient radiographic measurement parameters to be used as the standard in CCL rupture diagnosis.
Discussion
The differences within groups in the comparison of variables with versus those without TC were because joint stress caused by TC changed the anatomic position of the stifle. Of note, even though differences were present in some variables in all groups, these results are in agreement with the clinical hypothesis that joint stress caused by TC changed these variables in the following manner: increased patellar ligament angle, reduced patellar ligament insertion angle, and increased DPOI. The significance of the effect of TC for patellar ligament angle, patellar ligament insertion angle, and DPOI in G2 and G3 was expected, given that the projection with conventional positioning of the stifle might not exhibit clear evidence of cranial tibial translation in animals with CCL rupture10 and young dogs with physiological ligament laxity, whereas TC renders cranial tibial displacement more evident.
The lack of a difference between the means for G1 and G2 (P = .3027) is in agreement with the result from studies8,11 that show the variation in PLA is not significant when dogs with and without CCL rupture are compared. There is no significant difference in this variable between G1 and G3 (P = .1500) and between G2 and G3 (P = .3000). It shows that this parameter is not useful for the evaluation of CCL rupture and was unable to differentiate tibial translation in dogs with ligament rupture from healthy adult dogs and puppies.
The mean radiographic ATTa in healthy dogs without TC was 61.77°, which is above the mean of 57.4° found in a previous study.9 This might be due to radiographic positioning because the present study used a 135° stifle angle and the cited study used a 90° angle. The standardization of radiographic positioning is fundamental for comparisons among studies, and the difference between these studies is proof of this need. The stifle joint positioned at 135° attempts to mimic the weight-bearing position in dogs, thus rendering it more precise in the evaluation of cranial tibial translation parameters, as stated in some studies.9,12 Because this parameter was first established in the present study, the ATTb results cannot be compared with any data from the literature; however, these data will prove useful for future comparative studies and clinical applications.
The angle of cranial tibial translation has been described in only 1 study and only in healthy dogs, with no comparison whatsoever. Nevertheless, this study9 serves as a basis for future comparative studies. The ATTb is a modification proposed in the present study and, according to statistical analyses, can be included in the evaluation of tibial translation and used for comparisons between patients and between radiographic positioning methods. Overall, even though its values varied according to changes in the ATTa and both variables exhibited P values < .0001, the ATTb demonstrates the advantage over the conventional ATTa method, as it is simpler to measure the tibial translation angle since 1 less line is needed to obtain this measurement. In general, among the assessed angles and according to statistical analysis, the ATTa, the ATTb, and the patellar ligament insertion angle should be considered together due to the notable differences found in G2; however, there is no diagnostic impact on performing TC regarding the angles of tibial translation. Measuring the ATTa and the ATTb is more complex, and thus, diagnosis via patellar ligament insertion angle and DPOI measurements is simpler and more objective.
There is no description regarding the expected DPOI measures in relation to body weight or breed in dogs, and there is no information regarding a mathematical ratio to render this variable more reliable and eliminate the bias of dog size in the diagnosis of tibial translation in dogs with CCL rupture. In 1 study,13 the authors quantified cranial tibial translation in millimeters in dogs with CCL rupture, comparing measures obtained in a conventional manner with those obtained using the common tangent method; however, the above authors did not relate these results to healthy dogs. The DPOI measure is more often found in studies aimed at assessing the efficiency of surgical treatment by comparing radiographic images of the same patient throughout the course of the postoperative period.14
The DPOI ratio, obtained from conventional radiographs and those taken under TC, proved to be sufficient to add a very high degree of accuracy to the diagnosis of CCL rupture. Even though dogs with a predetermined body weight range were assessed in the present study, the results might be extrapolated to dogs of all sizes. However, for more precise analyses, patient values for different weight ranges and, even more specifically, for different breeds should be experimentally determined. In this case, DPOI ratio can be extrapolated with higher efficiency because it eliminates the bias of animal size and the comparative value of this ratio does not change due to size. Thus, a DPOI ratio value of 1.18 can be considered a standard index for the diagnosis of CCL rupture, according to the results obtained in the present study.
One limitation of this study is that radiography was performed under no sedation or anesthesia of the patient, which might have hindered adequate positioning of some more agitated or aggressive dogs. In the present study, only dogs with a surgically confirmed complete CCL rupture were included, and those with a partial rupture, possibly exhibiting only a torn craniomedial or caudolateral band, were excluded. Further studies are needed to compare such measurements in patients with complete and partial CCL rupture, aiming to identify a cutoff point to separate these groups.
Acknowledgments
The authors declare that there were no conflicts of interest.
The authors thank the Federal University of Lavras and the CAPES for the master’s scholarship.
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