Medial patellar luxation grade IV according to the Singleton system can be classified into skeletally immature and skeletally matured types

Yukari Nagahiro Laboratory of Veterinary Surgery, Faculty of Veterinary Medicine, Nippon Veterinary and Life Science University, Tokyo, Japan

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Sawako Murakami Laboratory of Veterinary Surgery, Faculty of Veterinary Medicine, Nippon Veterinary and Life Science University, Tokyo, Japan

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Masakazu Shimada Laboratory of Veterinary Surgery, Faculty of Veterinary Medicine, Nippon Veterinary and Life Science University, Tokyo, Japan

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Haruno Inoue Laboratory of Veterinary Surgery, Faculty of Veterinary Medicine, Nippon Veterinary and Life Science University, Tokyo, Japan

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Aki Tanaka Laboratory of Veterinary Surgery, Faculty of Veterinary Medicine, Nippon Veterinary and Life Science University, Tokyo, Japan

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Nobuo Kanno Laboratory of Veterinary Surgery, Faculty of Veterinary Medicine, Nippon Veterinary and Life Science University, Tokyo, Japan

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Yasuji Harada Laboratory of Veterinary Surgery, Faculty of Veterinary Medicine, Nippon Veterinary and Life Science University, Tokyo, Japan

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Yasushi Hara Laboratory of Veterinary Surgery, Faculty of Veterinary Medicine, Nippon Veterinary and Life Science University, Tokyo, Japan

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Abstract

OBJECTIVE

To determine the signalment and musculoskeletal morphology of small-breed dogs affected by medial patellar luxation (MPL) grade IV based on the age of the CT scan.

ANIMALS

40 small-breed dogs (54 limbs) with MPL grade IV.

PROCEDURES

Dogs that had undergone corrective surgery for MPL grade IV and had performed CT of the hind limb before surgery were included. Signalment (age, body weight, sex, laterality, and breed) and concomitant cranial cruciate ligament rupture (CrCLR) were recorded. Femoral inclination angle, anatomical lateral distal femoral angle (aLDFA), femoral torsion angle, quadriceps muscle length to femoral length ratio (QML/FL), and patellar ligament length to patellar length were obtained by CT images. The dogs were categorized into 2 groups based on their age at the time of the CT scan, the skeletally immature group and the skeletally matured group. Signalment and group were included in the multiple regression analysis to determine the factors associated with each measurement parameter. A logistic regression analysis was conducted to determine the risk of CrCL concomitant with age.

RESULTS

The multiple regression model demonstrated that the group was associated with the value of aLDFA and QML/FL. aLDFA was higher, and QML/FL was lower in group SI than in group SM. CrCLR was present in 5/54 limbs (9.2%), with a mean age of 70.8 months and it was associated with increasing age.

CLINICAL RELEVANCE

In Singleton’s classification, dogs classified as grade IV can be categorized into 2 groups based on musculoskeletal morphology and pathophysiology: the skeletally immature and skeletally matured types.

Abstract

OBJECTIVE

To determine the signalment and musculoskeletal morphology of small-breed dogs affected by medial patellar luxation (MPL) grade IV based on the age of the CT scan.

ANIMALS

40 small-breed dogs (54 limbs) with MPL grade IV.

PROCEDURES

Dogs that had undergone corrective surgery for MPL grade IV and had performed CT of the hind limb before surgery were included. Signalment (age, body weight, sex, laterality, and breed) and concomitant cranial cruciate ligament rupture (CrCLR) were recorded. Femoral inclination angle, anatomical lateral distal femoral angle (aLDFA), femoral torsion angle, quadriceps muscle length to femoral length ratio (QML/FL), and patellar ligament length to patellar length were obtained by CT images. The dogs were categorized into 2 groups based on their age at the time of the CT scan, the skeletally immature group and the skeletally matured group. Signalment and group were included in the multiple regression analysis to determine the factors associated with each measurement parameter. A logistic regression analysis was conducted to determine the risk of CrCL concomitant with age.

RESULTS

The multiple regression model demonstrated that the group was associated with the value of aLDFA and QML/FL. aLDFA was higher, and QML/FL was lower in group SI than in group SM. CrCLR was present in 5/54 limbs (9.2%), with a mean age of 70.8 months and it was associated with increasing age.

CLINICAL RELEVANCE

In Singleton’s classification, dogs classified as grade IV can be categorized into 2 groups based on musculoskeletal morphology and pathophysiology: the skeletally immature and skeletally matured types.

Medial patellar luxation (MPL) is one of the most common orthopedic diseases frequently occurring in small-breed dogs.13 The causes of MPL have not been fully defined, but they are classified as congenital, developmental, and traumatic.1 The impact of MPL on hindlimb movement varies markedly among individual dogs. In some dogs, MPL is diagnosed without obvious clinical signs (occult MPL)4 while others have a variety of clinical signs including severe lameness accompanied by femoral and tibial deformities during the growth period. Middle-to-older aged dogs show further loss of patellar stability, essentially worsening the grade of MPL or acute lameness because of concomitant cranial cruciate ligament rupture (CrCLR).

The MPL severity grading system proposed by Singleton, based on palpation of patellar luxation and difficulty of repositioning, has been widely used to the present day.5 In this classification, MPL grade IV is defined as the most severe stage in which the patella is always luxated medial to the femoral trochlear and cannot be repositioned manually into the femoral trochlear sulcus. Previous reports have shown that femoral varus, torsional, and tibial deformities accompany dogs with MPL grade IV,58 and there is a higher incidence of secondary CrCLR in middle-to-older aged dogs with a chronic course of MPL grade IV.3

The decision on appropriate treatment for MPL is based on the dog’s age, clinical symptoms, and the severity of the femoral and tibial morphological deformities. In recent years, preoperative CT imaging has been used frequently to assess morphological bone deformity,9 and several reports have compared the morphological values of the femur for each grade of patellar luxation.6,8,10 We also found that the quadriceps muscle length to femoral length ratio (QML/FL) increases with increasing age in MPL-affected dogs and that in grade IV-affected stifle joints, QML/FL was significantly lower than that of other grades.11 However, there were individual differences in age, femoral deformity, and QML/FL.12 Even if the stifle joint is diagnosed as MPL grade IV, these dogs are of varied age and have a wide range of pathologies, including the presence or absence of deformities of the femur and tibia and concomitant CrCLR. Although the musculoskeletal morphology may vary among individual dogs with MPL grade IV, no reports have been subdivided according to their musculoskeletal morphology. Therefore, in a retrospective study, we investigated the signalment and preoperative musculoskeletal morphology of dogs with MPL grade IV. We hypothesized that dogs with MPL grade IV have different types of hindlimb musculoskeletal morphology depending on the time of onset.

Materials and Methods

Inclusion criteria

Between April 2008 and December 2021, dogs with MPL grade IV who visited Nippon Veterinary and Life Science University Animal Hospital were included. The inclusion criteria were corrective surgery for MPL grade IV at our hospital and CT of the hind limb before surgery. Limbs that had a history of surgery for MPL grade IV or on the ipsilateral hip, femur, tibia, tarsal joints, and metatarsals before the visit to our hospital and limbs with incomplete medical records were excluded. “MPL grade IV” in Singleton’s classification was diagnosed by palpation.5 Signalment (age, body weight, sex, laterality, and breed), concomitant CrCLR, and preoperative CT data were reviewed from the medical records. Age and body weight were collected at the time of CT imaging. The femoral inclination angle (FIA), anatomical lateral distal femoral angle (aLDFA), femoral torsion angle (FTA), quadriceps muscle length to femoral length ratio (QML/FL), and patellar ligament length to patellar length (PLL/PL) were recorded from the CT images. The diagnosis of the CrCLR was tentatively made by the cranial drawer test and the tibial compression test.13,14 The final decision was made visually during the surgery.

Groups

According to previous reports about the growth of the femur,1518 dogs were classified into 2 groups based on the age at the CT scan of 10 months: the skeletally immature group (group SI) and the skeletally matured group (group SM). Group SI included dogs at 4–9 months of age at a CT scan. Namely, dogs affected with MPL grade IV at less than 10 months of age from birth were included. Group SM included dogs at 10 months or older at CT scan. Namely, dogs diagnosed with MPL grades IV at our hospital at age 10 months or older.

Anesthetic protocol

All dogs were under general anesthesia using the standard protocol at our hospital. The dogs were premedicated with midazolam (0.2–0.3 mg/kg, IM) or droperidol (0.25 mg/kg, IM), and propofol (to effect, IV) was used for anesthetic induction. Following intubation, anesthesia was maintained with isoflurane and 100% oxygen.

CT evaluation

All dogs were held in dorsal recumbency and fixed to maintain the hip and stifle joints at approximately 90°, respectively. CT imaging of the entire hindlimbs was performed. CT imaging was performed using a TSX-303A device (Toshiba) with a tube voltage of 120 kV, tube current of 150–300 mAs, slice width of 0.5–2.0 mm, and slice interval of 0.5–1.0 mm. All images were created and measured using AZE Virtual Place (AZE Corporation), which enables 3D and 2D measurements. Specific direction views of volume rendering (VR) images were used to assess the femoral joint orientation angles; FIA, FTA, and aLDFA. For QML/FL and PLL/PL evaluation, VR images and multi-planar reconstruction (MPR) images were used. Each length was measured using a 3D measurement tool on VR images. As the measurement lines were visible in all the images, the positioning in 3D space was confirmed by rotating the VR and MPR images.

Measurement parameters

Femoral joint orientation angles—For FIA or aLDFA measurement, VR frontal plane images of the femur were used. The FIA was defined as the angle formed by the femoral anatomical axis, that is, the line connecting the midpoints of the femur at the proximal 1/3 and 1/2 of the femoral length and the line passing through the point bisecting the center of the femoral head and the femoral neck. The aLDFA was defined as the angle formed by the femoral anatomical axis and the distal joint reference line connecting the most distal ends of the femoral medial and lateral condyles (Figure 1). An axial plane image was obtained by rotating the VR frontal plane images 90° dorsally for FTA measurement. The FTA was defined as the angle formed by the line connecting the center of the femoral head and neck and the line tangent to the caudal articular surface of the femoral condyle (Figure 1).6,19,20

Figure 1
Figure 1

Measurements of femoral joint orientation angles, quadriceps muscle length, femoral length, patellar ligament length, and patellar length. (A) Volume rendering (VR) frontal plane of CT image of femur. The femoral inclination angle (FIA) was defined as the angle formed by the femoral anatomical axis, the line connecting the midpoints of the femur at the proximal 1/3 and 1/2 of the femoral length (red dots) and the line passing through the point bisecting the center of the femoral head and the femoral neck. The anatomical lateral distal femoral angle (aLDFA) was defined as the angle formed by the femoral anatomical axis and the distal joint reference line connecting the most distal ends of the femoral medial and lateral condyle. (B) VR axial plane of CT image obtained by rotating (A) 90° dorsally. The red dots are where the 1/2 and 1/3 positions in (A) overlap, and the yellow angle brackets mean parallel lines. The femoral torsion angle (FTA) was defined as the angle formed by the line connecting the center of the femoral head and neck and the line tangent to the caudal articular surface of the femoral condyle. (C) VR image of the pelvis to the femur. Quadriceps muscle length (QML) was defined as the distance from the lateral area of the rectus femoris muscle on the iliac crest to the proximal patella. Femoral length (FL) was defined as the distance from the proximal greater trochanter of the femur to the long extensor tendon fossa of the lateral femoral condyle. (D) VR image of stifle joint. Patellar ligament length (PLL) was defined as the distance from the most distal point of the patella to the patellar ligament insertion point on the tibial tuberosity, and patellar length (PL) as the distance from the most proximal point to the most distal point of the patella. CT MPR images were used to determine the position of QML, FL, PLL, and PL in 3D space. The AZE virtual place 3D measurement tool was used to measure each length.

Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0020

QML/FL—QML was defined as the distance from the lateral area of the rectus femoris muscle on the iliac crest to the proximal patella. FL was defined as the distance from the proximal greater trochanter of the femur to the long extensor tendon fossa of the lateral femoral condyle (Figure 1). The QML/FL was calculated by dividing QML by FL.11,21

PLL/PL—PLL was defined as the distance from the most distal point of the patella to the patellar ligament insertion point on the tibial tuberosity, and PL was defined as the distance from the most proximal point to the most distal point of the patella (Figure 1). The PLL/PL was calculated by dividing the PLL by the PL.6,11,2124

Statistical analysis

First, we created scatter plots of the relationship between the age in months at the time of the CT scan and each measurement parameter. Next, a priori power analysis was performed. We set alpha at 0.05, power at 0.8, R2 at 0.4 for the full model and 0.25 for the reduced model, the total number of variables at 5, and the number being tested is 1, resulting in an estimated sample size of 34. The Shapiro–Wilk test was used to check the normality of each dataset, and then multiple regression analysis was conducted using each measurement parameter as the dependent variable and age, group, body weight, sex, laterality, and breeds as explanatory variables. After that, we conducted a post hoc analysis to confirm the normality of the residues. In addition, the logistic regression analysis was conducted to calculate the odds ratio (OR) with 95% CI for the risk of concomitant CrCL associated with age. All statistical analyses were performed using STATA 16.0 (Stata Corp), and P < .05 was considered significant.

Results

Forty dogs (54 hindlimbs) met the initial inclusion criteria. The number of limbs was larger than the estimated sample size obtained using a priori power analysis. The median age was 15.50 (4–123) months, and the median body weight was 3.00 kg (1.05–10.7). There were 20 male and 20 female dogs; 15 had bilateral MPL grade IV, and 25 had unilateral MPL grade IV. The contralateral limbs of dogs with unilateral MPL grade IV were healthy (n = 3) or had grade I (n = 3), grade II (n = 6), and grade III (n = 12) MPL; 1 dog had an incomplete medical record. In 1 dog with bilateral MPL grade IV, 1 limb was excluded because of a femoral neck fracture. Therefore, 54 limbs (29 left and 25 right sides) were assessed. The dog breeds were Toy Poodles (n = 17), Chihuahuas (n = 6), Pomeranians (n = 5), Shiba Inus (n = 4), mixes (n = 4), and others (n = 4) (Table 1). Group SI included 14 dogs (21 limbs), and group SM included 26 dogs (33 limbs). In group SI, the median age at the CT scan was 6 (4–9) months. In group SM, the median age at the CT scan was 24 (10–123) months. The median FIA, aLDFA, FTA, QML/FL, and PLL/PL for the SI group were 129.0° (range = 117.0–143.9°), 108.6° (range = 92.0–131.0°), 14.0° (range = 6.4–41.0°), 0.74 (range = 0.56–0.93), and 1.62 (range = 1.04–2.51), respectively. The median FIA, aLDFA, FTA, QML/FL, and PLL/PL for the SM group were 128.0° (range = 109.4–142.0°), 95.0° (range = 89.0–120.3°), 20.0° (range = 7.9–39.6°), 0.83 (range = 0.64–0.99), and 1.40 (range = 1.04–2.02), respectively (Table 1).

Table 1

Information and median (range) measurement parameters in group SI, group SM, and all dogs (n = 54).

Variables Group SI Group SM Total
Dogs (n) 14 26 40
Age: Median (range) (mo) 6.0 (4–9) 24.0 (10–123) 15.5 (4–123)
Body weight: Median (range) (kg) 2.6 (1.05–8.7) 3.15 (1.35–10.70) 3.00 (1.05–10.70)
Male (n) 7 13 20
Female (n) 7 13 20
Bilateral grade IV (n) 8 7 15
Unilateral grade IV (n) 6 19 25
Limbs (n) 21 33 54
Left limbs (n) 12 17 29
Right limbs (n) 9 16 25
Breeds
Toy poodle 7 dogs, 11 limbs 10 dogs, 13 limbs 17 dogs, 24 limbs
Chihuahua 1 dog, 1 limb 5 dogs, 5 limbs 6 dogs, 6 limbs
Pomeranian 1 dog, 1 limb 4 dogs, 5 limbs 5 dogs, 6 limbs
Shiba 3 dogs, 5 limbs 1 dog, 2 limbs 4 dogs, 7 limbs
Mix 1 dog, 2 limbs 3 dogs, 5 limbs 4 dogs, 7 limbs
Other 1 dog, 1 limb 3 dogs, 3 limbs 4 dogs, 4 limbs
Measurement parameters: Median (range)
FIA (°) 129.0 (117.0–143.9) 128.0 (109.4–142.0) 128.4 (102.8–143.9)
aLDFA (°) 108.6 (92.0–131.0) 95.0 (89.0–120.3) 99.0 (89.0–131.0)
FTA (°) 14.0 (-6.4–41.0) 20.0 (7.9–39.6) 19.0 (-6.4–41.0)
QML/FL 0.74 (0.56–0.93) 0.83 (0.64–0.99) 0.82 (0.56–0.99)
PLL/PL 1.62 (1.04–2.51) 1.40 (1.04–2.02) 1.48 (1.04–2.51)

aLDFA = Anatomical lateral distal femoral angle. FIA = Femoral inclination angle. FTA = Femoral torsion angle. PLL/PL = Patellar ligament length to patellar length ratio. QML/FL = Quadriceps muscle length to femoral length ratio.

A scatter plot of age and each measurement parameter showed that dogs of younger age at CT imaging tended to have a lower QML/FL and high aLDFA. Numerous dogs < 10 months of age had a QML/FL as extremely low as less than 0.8 and extremely high aLDFA as more than 100° (Figure 2). In the Shapiro-Wilk test, FIA, FTA, and QML/FL were normal, while aLDFA, PLL/PL were not normal. In multiple regression model for each measurement parameter demonstrated that QML/FL in the group SI was significantly lower than group SM (P = .002) and that aLDFA in the group SI was significantly higher than group SM (P = .027) (Table 2). Based on the most common breed, the toy poodle, statistical differences were found between it and specific other breeds in FIA, aLDFA, FTA, and PLL/PL (Table 2). In the post hoc analysis, the normality of the residue was confirmed. In addition, concomitant CrCLR present in 5/54 (9.2%), was not observed in group SI (0.0%) but was observed in 5 of 33 (15.2%) limbs in group SM with a mean age of 70.8 months. The logistic regression model showed that concomitant CrCLR was associated with increasing age (OR = 1.042, 95% CI [1.012–1.074], P = .005).

Figure 2
Figure 2

Scatter plots of age and each measurement parameter in all dogs. The red line marks 10 months; dogs of younger age at CT imaging tended to have a lower quadriceps muscle length/femoral length (QML/FL) and high anatomical lateral distal femoral angle (aLDFA). Numerous dogs < 10 months of age had a QML/FL as extremely low as less than 0.8 and extremely high aLDFA as more than 100°. aLDFA = Anatomical lateral distal femoral angle. FIA = Femoral inclination angle. FTA = Femoral torsion angle. PLL/PL = Patellar ligament length to patellar length ratio. QML/FL = Quadriceps muscle length to femoral length ratio.

Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0020

Table 2

Multiple regression model for each measurement parameter and signalment.

Dependent variables
FIA aLDFA FTA QML/FL PLL/PL
Explanatory variables Coefficient 95% CI P-value Coefficient 95% CI P-value Coefficient 95% CI P-value Coefficient 95% CI P-value Coefficient 95% CI P-value
Age −0.014 −0.126, 0.099 0.806 −0.086 −0.196, 0.023 0.120 0.0849 −0.040, 0.210 0.178 0.0004 −0.0006, 0.0013 0.449 −0.0028 −0.0065, 0.0009 0.140
Group (SM vs. SI) −5.306 −11.529, 0.917 0.093 −6.883 −12.944, −0.822 0.027* 4.822 −2.081, 11.725 0.166 0.0876 0.0346, 0.1406 0.002** −0.1517 −0.3576, 0.0542 0.145
Body weight 1.761 0.289, 3.232 0.020* 0.629 −0.805, 2.062 0.381 −1.126 −2.758, 0.506 0.171 0.0014 −0.0112, 0.0139 0.829 0.0322 −0.0165, 0.0809 0.189
Sex (Female vs. Male) −2.281 −7.784, 3.222 0.408 −1.265 −6.625, 4.095 0.637 −3.339 −9.444, 2.766 0.276 −0.0048 −0.0517, 0.0421 0.837 −0.0240 −0.2061, 0.1580 0.791
Laterality (Right vs. Left) −1.609 −6.368, 3.149 0.499 3.748 −0.886, 8.382 0.767 −2.518 −7.796, 2.760 0.341 −0.0064 −0.0470, 0.0341 0.750 0.0333 −0.1241, 0.1908 0.671
Breed (vs. Toy poodle)
Chihuahua 3.821 −4.431, 12.074 0.356 0.976 −7.061, 9.014 0.808 6.870 −2.284, 16.024 0.137 −0.0349 −0.1051, 0.0354 0.323 0.3665 0.0934, 0.6396 0.010*
Pomeranian −0.904 −9.888, 8.079 0.840 1.291 −7.458, 10.041 0.767 −0.336 −10.301, 9.629 0.946 −0.0502 −0.1267, 0.0263 0.193 0.1183 −0.1790, 0.4156 0.427
Shiba −4.244 −13.527, 5.039 0.362 −3.107 −12.149, 5.934 0.492 15.492 5.195, 25.790 0.004** −0.0116 −0.0907, 0.0675 0.769 0.2732 −0.0340, 0.5804 0.080
Mix −8.617 −17.009, −0.225 0.044* −7.042 −15.215, 1.132 0.089 2.644 −6.665, 11.953 0.570 0.0193 −0.0521, 0.0908 0.589 0.1111 −0.1666, 0.3888 0.424
Other −4.123 −13.630, 5.384 0.387 −9.896 −19.155, −0.636 0.037* −0.098 −10.644, 10.448 0.985 0.0248 −0.0562, 0.1058 0.540 −0.0209 −0.3355, 0.2937 0.894

aLDFA = Anatomical lateral distal femoral angle. FIA = Femoral inclination angle. FTA = Femoral torsion angle. PLL/PL = Patellar ligament length to patellar length ratio. QML/FL = Quadriceps muscle length to femoral length ratio.

*

P < 0.05.

**

P < 0.01.

Discussion

We compared dogs with MPL grade IV by dividing them into 2 groups based on the age at the CT scan: group SI (less than 10 months) and group SM (10 months or older). In 1966, Sumner-Smith reported that the fusion time of the distal femoral growth plate in dogs was 6–8 months of age.15 In 1973, Riser reported that axial growth of greyhound femurs slowed at 30 weeks of age, at which point 95% of the total growth length had been completed, and that the disappearance of the epiphyseal growth plate of the femur on radiographs occurred at 11–14 months.16 In 1980, Fukuda reported that the secondary ossification centers of the femur disappear at about 10 months.17 Α report by Berg in 1984 showed that femoral shortening was more severe with injuries at the distal epiphysis and that femoral shortening was more significant at younger ages.18 Although the time of skeletal maturity varies among breeds and individuals, we determined the age of 10 months as the borderline age based on these reports. The results showed differences between the 2 groups in the aLDFA, QML/FL, and rate of concomitant CrCLR. Therefore, we conclude that there are 2 types of dogs with MPL grade IV based on hind limb musculoskeletal morphology and pathophysiology: the skeletally immature and the skeletally matured types.

Measurements of aLDFA in healthy dogs and dogs with MPL have been reported (Table 3).68,10,25 Several reports showed that aLDFA is larger in MPL-affected dogs than in healthy dogs, especially in grade IV than in low-grade dogs.6,8,26 In this study, the median aLDFA of all dogs was 99.0°; of dogs in group SI was 108.6°, and of dogs in group SM was 95.0°. The multiple regression model showed that Group SI had significantly higher aLDFA than group SM (P = .027). As in a previous report, the aLDFA was higher in group SI dogs than in healthy dogs. Since the distal growth plate is responsible for 75% of the long-axial growth of the femur,16 if severe MPL develops in the early stages of skeletal development, especially between 10 and 30 weeks of age when long-axial growth is significant, the distal growth plate of the femur is affected. The medially displaced stifle extensor mechanism unit is placed at the shortest distance between its origin and termination, resulting in growth disturbance because of excessive forces on the medial part of the distal femoral growth plate, causing a growth disturbance secondary to femoral varus deformity and hypoplasia of the femoral medial condyle.27,28 In contrast, the median aLDFA of the dogs in group SM was similar to that of healthy dogs (Table 3). Most had a relatively small distal femoral deformity, while a few did not (Figure 2). The presence of dogs with relatively large bone deformities in the SM group suggests that they have had severe MPL during their skeletal development. Therefore, it showed that not all limbs affected by MPL grade IV have high aLDFA. However, those with permanent patellar luxation during skeletal development might have sustained changes in the distal femur, resulting in high aLDFA. Measurements of FIA and FTA in healthy dogs have also been reported (Table 3).68,10,25 Decreased FIA and changes in FTA have been reported as factors producing instability in the stifle joint.29 Although the values in both groups were similar to the mean values of healthy dogs, the relatively large range of minimum and maximum values confirmed the large individual differences (Figure 2, Table 1). Unlike previous reports, this study included a variety of breeds. Therefore, breed-specific femoral morphology might have caused large individual differences (Tables 2 and 3). The QML/FL has been reported to be 0.87–1.00 (mean ± SD; 0.93 ± 0.03) in healthy beagle dogs.21 In this study, the QML/FL tended to be lower in both groups than in healthy beagle dogs. Furthermore, a scatter plot of age and the QML/FL showed that the QML/FL tended to be lower in younger dogs, while numerous dogs < 10 months of age had a QML/FL as low as less than 0.8 (Figure 2). In dogs with MPL grade IV diagnosed at a younger age, the distal femoral growth plate might be damaged during growth. Simultaneously, a congenital malformation in the quadriceps muscle or a stunted quadriceps muscle might have induced femoral deformity and shortening of the QML. However, because the histopathology of the quadriceps muscle has not been evaluated, the cause has yet to be determined. PLL/PL has been associated with MPL in large breed dogs, and a ratio of PLL to PL (L:P) of 1.97 or more30 and PLL/PL of 2.06 or more indicated patella alta.23 Contrarily, PLL/PL was not associated with MPL in healthy dogs and dogs with MPL grades I–III in Pomeranians, Chihuahuas, and Poodles.24 In this study, the median PLL/PL for both groups was lower than the values of 1.73 to 2.0 for healthy and MPL-affected small-breed dogs.24 Furthermore, both groups had an extensive range of minimum-maximum values. In the previous reports, PLL/PL has been measured using lateral radiographs. In human medicine, evaluating the patellar ligament and patella using the Insall-Salvati ratio has been challenging to assess on radiographs in children during periods of incomplete ossification of cartilage, namely, the growth period.31 Additionally, because many dogs with MPL grade IV have an internal rotation of the proximal tibia or the tibia itself, we raise concerns of difficulty determining the exact location of the patellar ligament termination on the tibia on radiographs. Therefore, we used CT images for PLL and PL measurements to position the measurement points in 3D. The termination of the patellar ligament to the tibia was positioned at the caudal part of the patellar ligament. However, because of differences in the measurement modality and incomplete ossification depending on the dog’s age, the measurement sites may have differed slightly from those used in previous reports.6,2124 In addition, MPL grade IV was associated with patellar hypoplasia,6 and a large PLL/PL might have been caused by the smaller patella size. In the multiple regression model, PLL/PL was not associated with the age and groups. There have been no reports on PLL/PL during skeletal development in dogs, so further studies are needed to investigate the temporal changes in PLL/PL during skeletal development, differences according to breed or MPL grade, and the values measured using CT images.

Table 3

Femoral joint orientation angles of healthy dogs and dogs with medial patellar luxation grade IV reported previously.68,10,25

Breed Chihuahuas Toy Poodles Pomeranians Yorkshire Terriers Yorkshire Terriers
Author (year) Phetkaew (2018) Yasukawa (2016) Soparat (2012) Žilinčík (2018) Ševčík (2022)
Imaging modality CT CT Radiography Radiography Radiography
FIA normal 130.9 ± 4.4° 116.8 ± 6.1° 136.5 ± 7.1° 125.4 ± 4.1° 132.7 ± 2.9°
FIA grade IV 129.5 ± 6.9 118.3 ± 9.3 n/a 127 ± 4.2° n/a
FTA normal 29.2 ± 6.3° 19.8 ± 4.6° n/a 19.6 ± 2.9° n/a
FTA grade IV 21.1 ± 5.6 9.6 ± 5.2° n/a 9.2 ± 2.8° n/a
aLDFA normal 95.7 ± 3.6° 90.3 ± 2.8° 95.2 ± 3.5° 95.6 ± 2.1° 96.1 ± 2.2°
aLDFA grade IV 109.2 ± 9.7° 108.1 ± 8.0° n/a 110.2 ± 6.6° n/a

n/a = Not provided. See Table 1 for the remainder of the key.

The scatter plot shows that there were dogs with significantly lower QML/FL and significantly higher aLDFA in younger dogs. In contrast, there were fewer dogs with a low QML/FL or high aLDFA in older aged dogs. Without early surgical correction in congenital MPL, femoral varus deformity progresses during the skeletal development period.32 The younger the age at which the distal femoral growth plate is damaged, the more likely it is that severe femoral shortening will develop.18 Group SM included some dogs diagnosed with MPL grades I–III less than 10 months old at a private veterinarian but who had been followed up without treatment because of the absence of clinical symptoms, that is, occult MPL.4 Because the grade of MPL during the skeletal development period was milder than grade IV, the distal femoral growth plate was less likely to be damaged by the medial displacement of the stifle extensor mechanism unit. Group SM also included a relatively large number of middle-to-older-aged dogs. In these dogs, the medial trochlear cartilage ridge might have been damaged because of frequent luxation and repositioning of the patella at a younger age. Still, over time, the patella stabilized in the luxated position. It may have progressed to grade IV because of periarticular fibrosis associated with a chronic course of osteoarthritis and fibrous contracture of the medial joint capsule.33 Additionally, the internal rotation of the tibia may have contributed to the progression to grade IV in dogs with CrCLR secondary to MPL.3,34 In MPL, 15–20% of middle-to-older aged dogs, 22–48% of small-breed dogs, and 5/47 (10.6%) of MPL grade IV dogs have concurrent CrCLR.1,3,35,36 In this study, the logistic regression model showed concomitant CrCLR is associated with increasing age. Namely, it was more likely to occur in the older age; in group SM than in group SI. Skeletal deformity caused by MPL can lead to concomitant CrCLR by straining the CrCL3 or instability of the stifle joint, that is, increased internal range of motion of the tibia relative to the femur,36 leading to severe MPL. Furthermore, in habitual luxation of the patella, that is, MPL grade II, the tibia internally rotates about the femur during patellar luxation, and the tibia externally rotates to its normal position during patellar repositioning. Therefore, the CrCL is exposed to repetitive tension loading, which promotes chondrometaplasia of the CrCL and increases the risk of subsequent rupture.3,34 Femoral deformities in group SM were relatively small (Figure 3), showing that CrCLR might be induced by repetitive internal tension loading caused by MPL. As the CrCL can inhibit internal rotation of the tibia in the stifle joint of normal dogs,3739 CrCLR would have increased the range of internal rotation of the tibia, making the patella more likely to be permanently and irreparably luxated.

Figure 3
Figure 3

Radiographs and CT volume rendering images of the skeletally immature group and skeletally matured group. Upper: (A) medio-lateral view and (B) anterior-posterior view of the radiograph images and (C) volume rendering (VR) frontal plane of a CT image of a 5-month-old, 1.9 kg male Toy Poodle in the skeletally immature group. The patella is located proximal and medial to the trochlear. Additionally, varus deformity of the distal femur and proximal internal rotation of the tibia are observed. Bottom: (D) medio-lateral view and (E) anterior-posterior view of the radiograph images and (F) VR frontal plane of a CT image of a 15-month-old, 2.4 kg male Toy Poodle in the skeletally matured group. The patella is located medial to the trochlear. The tibia is internally rotated about the femur.

Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0020

The results of this study are valuable when considering surgical treatment for stifle joints affected by MPL grade IV. Stifle joints affected with MPL grade IV at less than 10 months of age with high aLDFA or a low QML/FL are more likely to require corrective osteotomy, that is, distal femoral osteotomy9 or segmental femoral osteotomy.12 Contrarily, stifle joints affected with MPL grade IV at 10 months or older are less likely to require such procedures.

There are several limitations to this study. First, although the time to skeletal maturity varies among breeds, differences between breeds were not considered. Additionally, the effects of femoral pro-recurvation and tibial deformity were not assessed simultaneously. Furthermore, linear measurement of FL in dogs with large aLDFA may underestimate the original FL because of the effect of femoral varus deformity. Moreover, there is uncertainty about the age at which the patient was affected by MPL grade IV.

In conclusion, in small-breed dogs with MPL grade IV, the aLDFA and QML/FL differ depending on age. The findings in this study support that dogs classified as grade IV in Singleton’s severity classification can be categorized into 2 groups based on musculoskeletal morphology and pathophysiology: the skeletally immature type and the skeletally matured type.

Acknowledgments

The authors declare that there were no conflicts of interest.

We would like to thank Editage (www.editage.com) for English language editing.

References

  • 1.

    Piermattei DL, Flo GL, DeCamp CE. The stifle joint. In: Brinker WO, Piermattei DL, Flo GL, eds. Handbook of Small Animal Orthopedics and Fracture Repair. 5th ed. Saunders Elsevier; 2016:597669.

    • Search Google Scholar
    • Export Citation
  • 2.

    Alam MR, Lee JI, Kang HS, et al. Frequency and distribution of patellar luxation in dogs. 134 cases (2000 to 2005). Vet Comp Orthop Traumatol. 2007;20(1):5964. doi:10.1055/s-0037-1616589

    • Search Google Scholar
    • Export Citation
  • 3.

    Campbell CA, Horstman CL, Mason DR, Evans RB. Severity of patellar luxation and frequency of concomitant cranial cruciate ligament rupture in dogs: 162 cases (2004-2007). J Am Vet Med Assoc. 2010;236(8):887891. doi:10.2460/javma.236.8.887

    • Search Google Scholar
    • Export Citation
  • 4.

    Hamilton L, Farrell M, Mielke B, Solano M, Silva S, Calvo I. The natural history of canine occult Grade II medial patellar luxation: an observational study. J Small Anim Pract. 2020;61(4):241246. doi:10.1111/jsap.13093

    • Search Google Scholar
    • Export Citation
  • 5.

    Singleton WB. The surgical correction of stifle deformities in the dog. J Small Anim Pract. 1969;10(2):5969. doi:10.1111/j.1748-5827.1969.tb04021.x

    • Search Google Scholar
    • Export Citation
  • 6.

    Yasukawa S, Edamura K, Tanegashima K, et al. Evaluation of bone deformities of the femur, tibia, and patella in Toy Poodles with medial patellar luxation using computed tomography. Vet Comp Orthop Traumatol. 2016;29(1):2938. doi:10.3415/VCOT-15-05-0089

    • Search Google Scholar
    • Export Citation
  • 7.

    Soparat C, Wangdee C, Chuthatep S, Kalpravidh M. Radiographic measurement for femoral varus in Pomeranian dogs with and without medial patellar luxation. Vet Comp Orthop Traumatol. 2012;25(3):197201. doi:10.3415/VCOT-11-04-0057

    • Search Google Scholar
    • Export Citation
  • 8.

    Phetkaew T, Kalpravidh M, Penchome R, Wangdee C. A Comparison of angular values of the pelvic limb with normal and medial patellar luxation stifles in Chihuahua dogs using radiography and computed tomography. Vet Comp Orthop Traumatol. 2018;31(2):114123. doi:10.3415/VCOT-17-05-0067

    • Search Google Scholar
    • Export Citation
  • 9.

    Brower BE, Kowaleski MP, Peruski AM, et al. Distal femoral lateral closing wedge osteotomy as a component of comprehensive treatment of medial patellar luxation and distal femoral varus in dogs. Vet Comp Orthop Traumatol. 2017;30(1):2027. doi:10.3415/VCOT-16-07-0103

    • Search Google Scholar
    • Export Citation
  • 10.

    Žilinčík M, Hluchý M, Takáč L, Ledecký V. Comparison of radiographic measurements of the femur in Yorkshire Terriers with and without medial patellar luxation. Vet Comp Orthop Traumatol. 2018;31(1):1722. doi:10.3415/VCOT-17-01-0018

    • Search Google Scholar
    • Export Citation
  • 11.

    Nagahiro, Y, Murakami, S, Shimada, M, Kanno, N, Harada, Y, Hara, Y. Evaluation of the quadriceps muscle length to femoral length ratio in small breed dogs with medial patellar luxation. Veterinary Surgery. 2023; 112. doi:10.1111/vsu.13951

    • Search Google Scholar
    • Export Citation
  • 12.

    Nagahiro Y, Murakami S, Kamijo K, et al. Segmental femoral ostectomy for the reconstruction of femoropatellar joint in dogs with grade IV medial patellar luxation. Vet Comp Orthop Traumatol. 2020;33(4):287293. doi:10.1055/s-0040-1709466

    • Search Google Scholar
    • Export Citation
  • 13.

    Arnoczky SP, Marshall JL. The cruciate ligaments of the canine stifle: an anatomical and functional analysis. Am J Vet Res. 1977;38(11):18071814.

    • Search Google Scholar
    • Export Citation
  • 14.

    Henderson RA. The tibial compression mechanism: a diagnostic aid in stifle injuries. J Am Anim Hosp Assoc. 1978;14(4):474479.

  • 15.

    Sumner-Smith G. Observations on epiphyseal fusion of the canine appendicular skeleton. J Small Anim Pract. 1966;7(4):303311. doi:10.1111/j.1748-5827.1966.tb04447.x

    • Search Google Scholar
    • Export Citation
  • 16.

    Riser WH. Growth and development of the normal canine pelvis, hip joints and femurs from birth to maturity: a radiographic study. Vet Radiol. 1973;14:2434. doi:10.1111/j.1740-8261.1973.tb00654.x

    • Search Google Scholar
    • Export Citation
  • 17.

    Fukuda S, Matsuoka O. Comparative studies on maturation process of secondary ossification centers of long bones in the mouse, rat, dog and monkey. Jikken Dobutsu. 1980;29(3):317326.

    • Search Google Scholar
    • Export Citation
  • 18.

    Berg RJ, Egger EL, Konde LJ, et al. Evaluation of prognostic factors for growth following distal femoral physeal injuries in 17 dogs. Vet Surg. 1984;13(3):172180. doi:10.1111/j.1532-950X.1984.tb00784.x

    • Search Google Scholar
    • Export Citation
  • 19.

    Towle HA, Griffon DJ, Thomas MW, Siegel AM, Dunning D, Johnson A. Pre- and postoperative radiographic and computed tomographic evaluation of dogs with medial patellar luxation. Vet Surg. 2005;34(3):265272. doi:10.1111/j.1532-950x.2005.00040.x

    • Search Google Scholar
    • Export Citation
  • 20.

    Dudley RM, Kowaleski MP, Drost WT, Dyce J. Radiographic and computed tomographic determination of femoral varus and torsion in the dog. Vet Radiol Ultrasound. 2006;47(6):546552. doi:10.1111/j.1740-8261.2006.00184.x

    • Search Google Scholar
    • Export Citation
  • 21.

    Murakami S, Nagahiro Y, Shimada M, et al. Effect of limb position on measurements of the quadriceps muscle length/femoral length ratio in normal Beagle dogs. Vet Comp Orthop Traumatol. 2020;33(4):279286. doi:10.1055/s-0040-1702235

    • Search Google Scholar
    • Export Citation
  • 22.

    Johnson AL, Probst CW, DeCamp CE, Rosenstein DS, Hauptman JG, Kern TL. Vertical position of the patella in the stifle joint of clinically normal large-breed dogs. Am J Vet Res. 2002;63(1):4246. doi:10.2460/AJVR.2002.63.42

    • Search Google Scholar
    • Export Citation
  • 23.

    Mostafa AA, Griffon DJ, Thomas MW, Constable PD. Proximodistal alignment of the canine patella: radiographic evaluation and association with medial and lateral patellar luxation. Vet Surg. 2008;37(3):201211. doi:10.1111/j.1532-950X.2008.00367.x

    • Search Google Scholar
    • Export Citation
  • 24.

    Wangdee C, Theyse LF, Hazewinkel HA. Proximo-distal patellar position in three small dog breeds with medial patellar luxation. Vet Comp Orthop Traumatol. 2015;28(4):270273. doi:10.3415/VCOT-15-02-0028

    • Search Google Scholar
    • Export Citation
  • 25.

    Ševčík K, Hluchý M, Ševčíková M, Domaniža M, Ledecký V. Inter- and intra-observer variations in radiographic evaluation of pelvic limbs in Yorkshire Terriers with cranial cruciate ligament rupture and patellar luxation. Vet Sci. 2022;9(4):179. doi:10.3390/vetsci9040179

    • Search Google Scholar
    • Export Citation
  • 26.

    Perry KL, Adams RJ, Andrews SJ, Tewson C, Bruce M. Impact of femoral varus on complications and outcome associated with corrective surgery for medial patellar luxation. Vet Comp Orthop Traumatol. 2017;30(4):288298. doi:10.3415/VCOT-16-09-0132

    • Search Google Scholar
    • Export Citation
  • 27.

    Hulse DA. Pathophysiology and management of medial patellar luxation in the dog. Vet Med Small Anim Clin. 1981;76(1):4351.

  • 28.

    Yasukawa S, Edamura K, Tanegashima K, et al. Morphological analysis of bone deformities of the distal femur in Toy Poodles with medial patellar luxation. Vet Comp Orthop Traumatol. 2021;34(5):303311. doi:10.1055/s-0041-1726084

    • Search Google Scholar
    • Export Citation
  • 29.

    Kowaleski MP, Boudrieau RJ, Pozzi A. Stifle joint. In: Tobias KM, Johnston SA, eds. Veterinary Surgery: Small Animal. 2nd ed. Elsevier; 2017:10711168.

    • Search Google Scholar
    • Export Citation
  • 30.

    Johnson AL, Broaddus KD, Hauptman JG, Marsh S, Monsere J, Sepulveda G. Vertical patellar position in large-breed dogs with clinically normal stifles and large-breed dogs with medial patellar luxation. Vet Surg. 2006;35(1):7881. doi:10.1111/j.1532-950X.2005.00115.x

    • Search Google Scholar
    • Export Citation
  • 31.

    Park MS, Chung CY, Lee KM, Lee SH, Choi IH. Which is the best method to determine the patellar height in children and adolescents. Clin Orthop Relat Res. 2010;468(5):13441351. doi:10.1007/s11999-009-0995-3

    • Search Google Scholar
    • Export Citation
  • 32.

    Nagaoka K, Orima H, Fujita M, Ichiki H. A new surgical method for canine congenital patellar luxation. J Vet Med Sci. 1995;57(1):105109. doi:10.1292/jvms.57.105

    • Search Google Scholar
    • Export Citation
  • 33.

    Roush JK. Canine patellar luxation. Vet Clin North Am Small Anim Pract. 1993;23(4):855868. doi:10.1016/S0195-5616(93)50087-6

  • 34.

    Vasseur PB. Stifle joint. In: Slatter D, ed. Textbook of Small Animal Surgery. 3rd ed. Saunders, 2003;20902133.

  • 35.

    Andrade MC, Slunsky P, Klass LG, Brunnberg L. Risk factors and long-term surgical outcome of patellar luxation and concomitant cranial cruciate ligament rupture in small breed dogs. Vet Med (Praha). 2020;65:159167. doi:10.17221/155/2019-VETMED

    • Search Google Scholar
    • Export Citation
  • 36.

    Hans EC, Kerwin SC, Elliott AC, Butler R, Saunders WB, Hulse DA. Outcome following surgical correction of grade 4 medial patellar luxation in dogs: 47 stifles (2001-2012). J Am Anim Hosp Assoc. 2016;52(3):162169. doi:10.5326/JAAHA-MS-6329

    • Search Google Scholar
    • Export Citation
  • 37.

    Arnoczky SP, Torzilli PA, Marshall JL. Biomechanical evaluation of anterior cruciate ligament repair in the dog: an analysis of the instant center of motion. J Am Anim Hosp Assoc. 1977;13(5):553558.

    • Search Google Scholar
    • Export Citation
  • 38.

    Shimada M, Takagi T, Kanno N, et al. Biomechanical effects of tibial plateau levelling osteotomy on joint instability in normal canine stifles: an in vitro study. Vet Comp Orthop Traumatol. 2020;33(5):301307. doi:10.1055/s-0040-1709505

    • Search Google Scholar
    • Export Citation
  • 39.

    Shimada M, Takagi T, Kanno N, Yamakawa S, Fujie H, Hara Y. Influence of tibial plateau levelling osteotomy on the tensile forces sustained by ligaments in cranial cruciate ligament-intact canine stifles: an ex vivo pilot study. Vet Med Sci. 2022;8(5):19041914. doi:10.1002/vms3.889

    • Search Google Scholar
    • Export Citation
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