Quantitative assessment of hip morphology to enhance the identification of hip dysplasia in German Shepherd Dogs

Ayman A. Mostafa Department of Small Animal Surgery and Radiology, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt

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Clifford R. Berry Diagnostic Imaging, Department of Molecular Biomedical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC

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Menna A. Nahla Department of Small Animal Surgery and Radiology, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt

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Abstract

OBJECTIVE

To develop quantitative measures that, when combined with the Fédération Cynologique Internationale (FCI) score, would potentially enhance the accuracy of the scoring process.

ANIMALS

153 client-owned purebred German Shepherd Dogs with normal and near normal (71 dogs) and dysplastic coxofemoral joint (82 dogs).

PROCEDURES

Center edge (CE) angle, Norberg angle (NA), indexes of dorsal acetabular femoral head (AFH) coverage width and area, acetabular index angle, and inclination angle were determined. We also investigated the correlation between selected variables. Coxofemoral joints were classified into normal, near normal, and mildly, moderately, and severely dysplastic joints based on the morphometric criteria previously established by the conventional FCI scoring. Variables were compared among the 5 groups using ANOVA. Linear relationships were determined using Spearman correlation coefficients.

RESULTS

All radiographic measurements differed significantly (P < .0001) among the 5 assigned groups (normal, near normal, mildly dysplastic, moderately dysplastic, and severely dysplastic hip joints). NA was the only measure that differed significantly (P ≤ .03) between the 5 assigned groups. Positive correlations were identified between Norberg and CE angles (rs = 0.93), between width and area indexes of dorsal AFH coverage (rs = 0.92), and between the measurement techniques utilized to assess lateral versus dorsal AFH coverage (rs ≥ 0.65).

CLINICAL RELEVANCE

Evaluation of lateral and dorsal AFH coverage may help to refine the scoring system used to select German Shepherd Dogs for breeding. German Shepherd Dogs with NA < 103°, CE angle < 20.8°, dorsal AFH coverage width index ≤ 49%, and/or dorsal AFH coverage area index ≤ 51% should be considered to have mild, moderate, or severe hip dysplasia and are therefore not good candidates for breeding. Borderline values between near normal and mildly dysplastic joints should be reevaluated.

Abstract

OBJECTIVE

To develop quantitative measures that, when combined with the Fédération Cynologique Internationale (FCI) score, would potentially enhance the accuracy of the scoring process.

ANIMALS

153 client-owned purebred German Shepherd Dogs with normal and near normal (71 dogs) and dysplastic coxofemoral joint (82 dogs).

PROCEDURES

Center edge (CE) angle, Norberg angle (NA), indexes of dorsal acetabular femoral head (AFH) coverage width and area, acetabular index angle, and inclination angle were determined. We also investigated the correlation between selected variables. Coxofemoral joints were classified into normal, near normal, and mildly, moderately, and severely dysplastic joints based on the morphometric criteria previously established by the conventional FCI scoring. Variables were compared among the 5 groups using ANOVA. Linear relationships were determined using Spearman correlation coefficients.

RESULTS

All radiographic measurements differed significantly (P < .0001) among the 5 assigned groups (normal, near normal, mildly dysplastic, moderately dysplastic, and severely dysplastic hip joints). NA was the only measure that differed significantly (P ≤ .03) between the 5 assigned groups. Positive correlations were identified between Norberg and CE angles (rs = 0.93), between width and area indexes of dorsal AFH coverage (rs = 0.92), and between the measurement techniques utilized to assess lateral versus dorsal AFH coverage (rs ≥ 0.65).

CLINICAL RELEVANCE

Evaluation of lateral and dorsal AFH coverage may help to refine the scoring system used to select German Shepherd Dogs for breeding. German Shepherd Dogs with NA < 103°, CE angle < 20.8°, dorsal AFH coverage width index ≤ 49%, and/or dorsal AFH coverage area index ≤ 51% should be considered to have mild, moderate, or severe hip dysplasia and are therefore not good candidates for breeding. Borderline values between near normal and mildly dysplastic joints should be reevaluated.

Canine hip dysplasia (CHD) is a developmental disorder of the coxofemoral joint accompanied by joint laxity and incongruity that may develop into coxarthrosis.1,2 The disease is prevalent in large-breed dogs that grow rapidly,3 including German Shepherd Dogs, Labrador Retrievers, and Boxers.4,5 A variety of radiographic measurements have been utilized in both adult humans and dogs to assess hip dysplasia.2,69 An extended ventrodorsal (VD) view of the pelvis, first introduced in the 1960s by Riser,10 is still used to examine the canine coxofemoral joint, according to the Fédération Cynologique Internationale (FCI), the Orthopedic Foundation for Animals, and the British Veterinary Association and the Kennel Club.11 The Norberg angle (NA) is a commonly used radiographic measurement in dogs to quantify the degree of lateral acetabular femoral head (AFH) coverage.12,13 However, this technique considers both coxofemoral joints. In humans, the center edge (CE) and acetabular index angles measured on the anteroposterior view are used to independently assess the degree of lateral AFH coverage and the steepness of the cranial acetabular edge, respectively, for each hip joint.6,7,14,15 Two reports identified the CE9,16 and acetabular index9 angles on the extended VD pelvic radiographs in dogs. However, these investigations relied on the contralateral hip joint to measure the CE angle using the long axis of the pelvis (the axis perpendicular to a line connecting the FH centers)16 or using the midsagittal axis.9 On the other hand, the acetabular index angle is used to measure the steepness of the weight-bearing surface of the cranial acetabulum (the thick bone of the cranial acetabular edge) in humans8 and dogs.9 Measurement of the acetabular index angle relies on the use of the transverse planes drawn in the supine position in humans and the dorsal recumbent position in dogs. Unlike human anteroposterior pelvic radiographs, canine VD pelvic radiographs are taken in the dorsal recumbent position; hence, a midsagittal or transverse axis may not be effective for measuring the CE or acetabular index angle. Furthermore, the previously estimated CE and acetabular index angles in the veterinary literature depended on both the right and left coxofemoral joints, because a line is drawn between the femoral head centers. The current study is the first to evaluate the CE and acetabular index angles for each hip joint independently and assess the degree of dorsal AFH coverage and the inclination angle (IA) in German Shepherd Dogs with normal and dysplastic hip joints. Existing selective breeding strategies, using conventional radiographic procedures such as the NA, have not significantly lowered the CHD levels.1720 Instead, the modified-FCI scoring system recently established in Labrador Retrievers provided morphometric criteria for each score to quantify the extent of lateral and dorsal AFH coverage, the steepness of cranial acetabular edge, and the IA in normal, near normal, and dysplastic joints.21 Therefore, our main objective is to develop a similar scoring system for the coxofemoral joint of German Shepherd Dogs to develop quantitative measures that, when combined with the FCI score, would potentially enhance the accuracy of the scoring process. To overcome the possible interbreed variability, both recent and current studies performed on Labrador Retrievers and German Shepherd Dogs, respectively, were carried out without combining the 2 populations. In the present study, we hypothesize that the AFH coverage, cranial acetabular edge steepness, and IA in dysplastic joints will differ from normal or near normal joints. Our long-term goal is to evaluate the effectiveness of the FCI after adding these modifications to develop an appropriate assessment protocol that, when applied to a selective breeding strategy using German Shepherd Dog parents with phenotypically normal coxofemoral joints at the time of assessment, lowers the prevalence of hip dysplasia among offspring. Thus, this protocol may encourage veterinarians and clinical practitioners to utilize it in an attempt to prevent the breeding of dogs without consideration of normal hip conformation at the time of breeding.

Materials and Methods

Animals

The Scientific Committee of the Department of Surgery and Radiology at the Faculty of Veterinary Medicine, Cairo University approved this retrospective study protocol before the investigation. Medical records and extended VD pelvic radiographs of adult German Shepherd Dogs with “normal” and dysplastic hip morphology were retrieved from the database of the Small Animal Hospitals at Cairo University and the University of Florida from May 2006 to March 2021. Ethical review and approval were not needed as the retrospective nature of the current study relied solely on the medical records reviews and radiographic images routinely generated during the veterinary care of our enrolled dogs. The quality and positioning of all digitized radiographs were approved according to the previously established criteria for the standard extended-leg ventrodorsal pelvic view.22,23 The dogs were categorized into 5 groups (A to E) by a qualified radiologist (AAM). The categorization was then approved and finalized by a board-certified radiologist (CRB). This categorization was achieved based on the morphometric criteria for CHD previously established by the conventional Fédération Cynologique Internationale (FCI) scoring protocol.24,25 The groups included normal (grade A) and near normal (grade B) joints and mildly (grade C), moderately (grade D), and severely (grade E) dysplastic joints. The grade A (normal joints) group exhibited coxofemoral joints with narrow space, sharply margined perfectly parallel articular surfaces (perfectly congruent joint), and NAs ≥ 105°. The grade B (near normal joints) group exhibited coxofemoral joints with sharply margined, nonparallel articular surfaces, slightly widened joint spaces (minimal joint incongruence), and NAs ≥ 105° or congruent coxofemoral joints with NAs < 105°. Hip joints in the grade C group were mildly dysplastic with incongruity of the coxofemoral joint (wedged-shaped joint space), a slightly flattened craniolateral acetabular rim, and a NA around 100°. The grade D group had moderately dysplastic hips with obvious joint incongruity and subluxation with associated flattening of the craniolateral acetabular rim and NAs < 100°. The grade E group exhibited severely dysplastic hips with coxofemoral luxation or distinct subluxation and flattening and/or deformity of the femoral head and/or acetabulum. The existence of a radiodense line extending from the base of the femoral neck to the trochanteric fossa (ie, new bone formation along the insertion of the joint capsule) or any radiographic evidence of coxofemoral osteoarthritis was recorded for dysplastic joints (grades C to E).11

Radiographic measurements

All radiographic measurements, including the previously measured NA, were performed once on digitized radiographs by the same investigator (MAN) who was blinded to the group allocation. Measurements were made using medical and radiologic image processing software (ImageJ 1.41/Java 1.6.0_21) at 200% magnification.12,13,26 The following radiographic parameters were used to evaluate the coxofemoral joints: (1) CE and NA, measuring the extent of lateral AFH coverage; (2) indexes of dorsal AFH coverage width and area, measuring dorsal AFH coverage; (3) acetabular index/slope angle, quantifying the cranial acetabular edge steepness; and (4) IA, evaluating the proximodistal alignment of the femoral head and neck relative to the corresponding femoral axis.

Initially, a best-fit circle was drawn around the femoral head to define its center and calculate its area. The NA and IA (method B) were measured as previously published.12,13,2729 The CE and acetabular index angles were measured using procedures modified from previously established human techniques.6,7,14,15,30 The CE angle was measured between 2 straight lines originating from the center of the femoral head; the first line was tangential to the dorsal acetabular rim and the second line was parallel to the longitudinal axis of the body of the corresponding ilium (iliac axis, a line bisecting the shaft of the ilium13; Figure 1). The acetabular index angle was formed between a line connecting the lateral and medial extents of the dense bone of the cranial acetabular edge (acetabular sourcil slope) and a horizontal line perpendicular to the corresponding iliac axis. Every angle was recorded to the nearest tenth of the corresponding calculated degree. The femoral head diameter was drawn perpendicular to and bisecting the corresponding dorsal acetabular edge to measure the width of the dorsal acetabulum that overlays the femoral head at this level (Figure 2). The width index of dorsal AFH coverage was then calculated by dividing the width of the dorsal acetabular coverage by the femoral head diameter. The area index of dorsal acetabular coverage was calculated by dividing the area of the femoral head covered by the corresponding dorsal acetabulum and bounded laterally by the dorsal acetabular edge by the overall femoral head area.

Figure 1
Figure 1

An extended ventrodorsal pelvic radiograph of a moderately dysplastic coxofemoral joint illustrating measurements of the center edge angle (Φ) (A) and the acetabular index angle (α) (B). a = Long axis of the iliac body. b = Line originating from the femoral head center and tangential to the lateral acetabular rim. c = Line tangential to the lateral and medial extents of the cranial acetabular rim (acetabular sourcil). d = Horizontal line perpendicular to the iliac axis (a).

Citation: American Journal of Veterinary Research 84, 3; 10.2460/ajvr.22.09.0165

Figure 2
Figure 2

An extended ventrodorsal pelvic radiograph of a moderately dysplastic coxofemoral joint, illustrating measurements of the dorsal acetabular femoral head (AFH) coverage width index (A) and the dorsal AFH coverage area index (B). w = Width of dorsal acetabular coverage. di = Diameter of the femoral head. a = Area of dorsal acetabular coverage; A = Area of the femoral head.

Citation: American Journal of Veterinary Research 84, 3; 10.2460/ajvr.22.09.0165

Statistical analysis

Data analyses were selected and performed by the first author (AAM). Data were analyzed using commercially available statistical software (Graph-Pad Prism version 8.00). Normality was determined using the Kolmogorov-Smirnov test. Mean (± SD) values and 95% CIs were calculated for selected measurements. Variables of interest were compared between the 5 groups using ANOVA and Tukey test. A P value < .05 was considered statistically significant. Spearman rank correlation coefficients (rs) were calculated to determine the linear relationships between selected variables. Correlation coefficients ranged from 0 to 1, with values from 0 to 0.30, 0.30 to 0.70, and 0.70 to 1.0 representing weak, moderate, and strong correlation, respectively.31

Results

Animals

Coxofemoral joints from 153 purebred German Shepherd Dogs (289 hip joints) were categorized as grade A (76 joints, 26.2%), grade B (49 joints, 17.0%), grade C (31 joints, 10.7%), grade D (69 joints, 23.9%), and grade E (64 joints, 22.2%). Sixty-two (21.5%) coxofemoral joints exhibited secondary osteoarthritis (39 severely, 18 moderately, and 5 mildly dysplastic joints). Subluxation was identified in 60 (20.8%) coxofemoral joints (50 severely and 10 moderately dysplastic joints). Luxated coxofemoral joints (17 joints, 5.9%) were excluded from the radiographic measurements. The Morgan line was identified in 46 (15.9%) coxofemoral joints (19 mildly, 14 moderately, and 13 severely dysplastic joints). Age and body weight did not differ (P ≥ .320) between groups (Supplementary Table S1). The female-to-male ratio was 1:1.1, including 81 males (35 castrated) and 72 females (38 spayed).

Radiographic measurements

As NA was utilized as a reference parameter to categorize our population into 5 assigned groups (A to E), it was the only measure that differed significantly (P ≤ .03, Tukey test) between every 2 consecutive groups (groups A vs B, B vs C, C vs D, and D vs E). All other radiographic measurements varied significantly among the 5 assigned groups (normal, near normal, mildly dysplastic, moderately dysplastic, and severely dysplastic coxofemoral joints) (P < .0001, ANOVA; Supplementary Table S1; Figure 3). The CE angle did not differ significantly between the near normal and mildly dysplastic hip joints (P = .248, Tukey test). No significant differences in the dorsal acetabular width or area indexes were detected between normal and near normal or between near normal and mildly dysplastic joints (P ≥ .125, Tukey test). The dorsal acetabular area index did not differ significantly between mildly and moderately dysplastic joints (P = .078, Tukey test). The acetabular index and inclination angle differed significantly in severely dysplastic joints compared to the other tested groups (P ≤ .001, Tukey test; Figure 4). However, no significant differences were detected in the acetabular index or inclination angles between normal versus near normal and mildly and moderately dysplastic joints, between near normal versus mildly and moderately dysplastic joints, or between mildly versus moderately dysplastic joints (P ≥ .300, Tukey test). The mean (± SD) values and 95% CIs for each variable are shown (Supplementary Table S1). A modified-FCI scoring protocol was developed based on the morphometric criteria and the results of the radiographic measurements for each group (Supplementary Table S2).

Figure 3
Figure 3

Box-and-whisker plots of Norberg angle (A), center edge angle (B), dorsal acetabular coverage width index (C), and dorsal acetabular coverage area index (D) for normal, near normal, mildly dysplastic, moderately dysplastic, and severely dysplastic coxofemoral joints.

Citation: American Journal of Veterinary Research 84, 3; 10.2460/ajvr.22.09.0165

Figure 4
Figure 4

Box-and-whisker plots of the acetabular index angle (A) and inclination angle (B) for normal, near normal, mildly dysplastic, moderately dysplastic, and severely dysplastic coxofemoral joints.

Citation: American Journal of Veterinary Research 84, 3; 10.2460/ajvr.22.09.0165

A strong positive correlation (rs = 0.93, P < .0001) was identified between the measurements utilized to radiographically evaluate the degree of lateral AFH coverage (ie, NA and CE angle; Figure 5). Also, a strong correlation (rs = 0.92, P < .0001) was detected between the 2 indexes (width and area) assessing the degree of dorsal AFH coverage. Moderate to strong correlations (rs ≥ 0.65, P < .0001) were observed between the radiographic techniques utilized to assess lateral versus dorsal AFH coverage (Figure 6). A moderate negative correlation (rs = −0.54, P < .0001) was identified between the acetabular index and CE angles. Moderate to weak correlations (rs ≤ 0.38) were identified between the IA and each of the reported radiographic measurements.

Figure 5
Figure 5

Scatterplots of the center edge angle versus Norberg angle (A) and dorsal acetabular coverage area index versus dorsal acetabular coverage width index (B) were determined for 289 normal and dysplastic coxofemoral joints from 153 purebred German Shepherd Dogs.

Citation: American Journal of Veterinary Research 84, 3; 10.2460/ajvr.22.09.0165

Figure 6
Figure 6

Scatterplots of the Norberg angle versus the dorsal acetabular coverage width index and the dorsal acetabular coverage area index (A and B), the center edge angle versus the dorsal acetabular coverage width index and the dorsal acetabular coverage area index (C and D), and the acetabular index angle versus the center edge angle (E) determined for 289 normal and dysplastic coxofemoral joints from 153 purebred German Shepherd Dogs.

Citation: American Journal of Veterinary Research 84, 3; 10.2460/ajvr.22.09.0165

Discussion

There are 3 major findings in this study. First, significant variations in all investigated radiographic measurements were identified among the 5 tested groups (normal, near normal, mildly dysplastic, moderately dysplastic, and severely dysplastic coxofemoral joints). The extent of lateral AFH coverage was higher in normal versus near normal coxofemoral joints; however, dorsal AFH coverage did not differ between the same 2 groups. Norberg or CE angles < 103° or < 20.8°, respectively, and dorsal AFH coverage width or area index < 49% or < 51%, respectively, were consistent with hip dysplasia. Second, the strong correlation (rs = 0.93) between the Norberg and CE angles supports using the CE angle as an alternative method to quantifying lateral AFH coverage without considering the contralateral side. Furthermore, the strong correlation (rs = 0.92) between the indexes of dorsal AFH coverage width and area supports the use of the width index as a simpler alternative method to quantify dorsal AFH coverage. Third, steep cranial acetabular edges (increased acetabular index angle) and coxa vara (decreased IA) were consistent with severely dysplastic coxofemoral joints.

A recent similar study21 performed on Labrador Retrievers revealed significant variations in all measurements among the 5 groups (grades A to E) of coxofemoral joints. However, the extent of both dorsal (width index) and lateral (Norberg and CE angles) AFH coverage did not differ between normal and near normal coxofemoral joints. In this previous report,21 strong correlations (rs ≥ 0.80) were also identified between the NA and CE angle, the width and area indexes of dorsal AFH coverage, and the procedures used to measure the lateral versus dorsal AFH coverage. In Labrador Retrievers, the Norberg or CE angles < 108° or < 27° and dorsal AFH coverage width or area index < 52% or < 53%, respectively, were consistent with hip joint incongruence and possible dysplasia.21 Moreover, a steep cranial acetabular edge and coxa vara were observed in Labrador Retrievers with moderate and severe hip dysplasia.21

In general, CE angle and Norberg angle (NA) assess the degree of lateral acetabular coverage of the corresponding femoral head. The means NA in group A (108.1°), group B (103.3°), group C (100.5°), group D (96.6°), and group E (80.7°) were relatively consistent with those reported previously (group A, 108.5°, 106.9°; group B, 105.85°, 104.6°; group C, 101°, 100.5°; group D, 95°, 93.2°; and group E 82.62°, 87.5°) (23,30). However, the means CE angle of the 5 tested groups (A to E) in the present study (26°, 21.5°, 19.4°, 15.9°, and −0.1°, respectively) differed from those reported by a previous prospective study performed on 208 hip joints of large- and giant-breed dogs (16.9°, 12.6°, 10.7°, 6.6°, and −9.3° respectively).25 This disparity may be related to the use of the iliac axis to assess the CE angle in the present study instead of the longitudinal axis utilized by such a previous study. Nonetheless, the normal and dysplastic CE angles reported in our investigation (25.3° and 20.3°, respectively) were similar to the normal and dysplastic CE angles reported in humans (25° and 20°, respectively),30,32,33 despite the anatomical and biomechanical differences between human and dogs. This supports the feasibility of using the corresponding iliac axis rather than the absolute long axis, which may not be realistic in the radiographic evaluation of a canine pelvis.13,32 There were strong correlations between the NA and CE angle identified in the present study (rs = 0.93) and a previous report investigated 208 hip joints of large- and giant-breed dogs (rs = 0.79).25 Accordingly, we advocate using the modified CE angle over the NA to assess the degree of lateral AFH coverage of each joint separately without considering the contralateral hip joint. This method may avoid the potential limitations related to NA described by the present study and reported by a previous retrospective study16 performed on 387 Leonberger dogs. In addition to the absolute dependence on the contralateral side to measure NA, its measurement procedure has been reported to be influenced more by the osteoarthritic changes and subluxation of the femoral head compared to that of CE angle.16

The extent of dorsal AFH coverage was evaluated in the current study by calculating the indexes of dorsal acetabular coverage width and area. The indexes of dorsal acetabular coverage area in the 5 groups (A to E) (56%, 53%, 50%, 46%, and 27%, respectively) were relatively consistent with the indexes (59.4%, 54.1%, 45.7%, 37.6%, and 28.2%, respectively) reported by a previous study34 evaluated 1841 large-breed dogs (Labrador Retrievers, Golden Retrievers, Rottweilers, and German Shepherd Dogs). The indexes of dorsal AFH coverage width and area reported in our near normal group (51% and 53%, respectively) agreed with the median values of linear and surface acetabular overlap (52% and 54%, respectively) previously reported8 for a wide variety of dog breeds. In the present study, the inability of the dorsal AFH coverage indexes (width and area indexes) to differentiate between normal versus near normal and near normal versus mildly dysplastic coxofemoral joints may be due to the similar dorsal acetabular coverage in these groups. The strong correlation (rs = 0.92) between the width and area indexes supports the use of the width index as a simpler alternative method for quantifying dorsal AFH coverage in German Shepherd Dogs. A similar correlation (rs = 0.84) between the 2 indexes was reported by a previous study8 carried out on 200 coxofemoral joints belonging to a wide variety of dog breeds. Thus, the authors encourage evaluation of both lateral (CE angle) and dorsal (width index) AFH coverage (ie, the overall AFH coverage), especially when evaluating German Shepherd Dogs prior to breeding.

The acetabular index angle indicates the steepness of the cranial acetabular edge (acetabular sourcil slope). The means acetabular index angles calculated for our 5 groups (A to E) (13.2°, 12.8°, 14.1°, 15.7°, and 29.1° respectively) were similar to those reported in a previous study25 (7.1°, 11.6°, 11.8°, 15.0°, and 25.2° respectively). The minimal variation in the acetabular index angle between the 2 studies may be related to the minimal difference between the 2 measuring techniques (ie, using the iliac axis versus the long axis). Excessive cranial acetabular edge steepness was observed in severely dysplastic coxofemoral joints. An acetabular slope angle > 13° (>14° in our tested German Shepherd Dogs) is most likely associated with hip dysplasia in humans.35 The significant difference in the hip joint standing angle between humans and dogs may reveal differences in the natural load applied to the acetabulum of each species.13,3638 The natural load applied to the cranial acetabular edge in humans may explain the excessive steepness of the cranial acetabular edge in dysplastic hips.35 However, the natural load applied to the dorsal acetabular region is expected to be greater than the load applied to the cranial acetabular region in dogs.12,13,38,39 This indicates the relevance of assessing both dorsal and lateral AFH coverage during routine canine hip joint screening. The negative correlation (rs = −0.54) between the acetabular index angle and the CE angle implies that a low steep acetabular roof is associated with a high lateral AFH coverage in normal hip joints. The means IA calculated for the normal and near normal coxofemoral joints of our investigated German Shepherd Dogs (130.5° and 129.8°, respectively) were consistent with the normal value (129.4°) previously reported in large-breed dogs.27,28 The decreased angle of inclination (coxa vara) in the present study indicates severely dysplastic coxofemoral joints. However, the IA failed to differentiate between the other 4 groups (A to D). The difference in the IA between dysplastic and healthy joints was insignificant in other studies.28,29 The disparity across studies might be attributed to the differences in the accompanying external femoral rotation, coxarthrosis, and/or coxofemoral luxation/subluxation, which may alter the IA, as described previously.29 German Shepherd Dogs with normal (grade A) and near normal (grade B) coxofemoral joints are expected to be included in our suggested breeding strategy. Thus, only dogs with mildly (grade C), moderately (grade D), and severely (grade E) dysplastic hips are advised to be excluded from breeding. This suggestion differs from that proposed by Flückiger40 who advised including dogs with mildly dysplastic joints with some restrictions during the selective breeding protocol.

The gap of values between every 2 consecutive groups (groups B vs C, C vs D, and D vs E) may represent subjects with borderline degrees of hip dysplasia (Supplementary Tables S1 and S2), which is a limitation of the current study. However, borderline results between different stages of hip dysplasia have been recorded in other veterinary and human studies.33,39 Therefore, we recommend a comprehensive assessment of AFH coverage (both dorsal and lateral), especially in animals with borderline degrees of hip dysplasia. Furthermore, a reevaluation of the coxofemoral joints with borderline values located between near normal and mildly dysplastic joints is recommended after 6 months, as previously advised by Flückiger40 in 2007. Another limitation of the current study is the absence of a repeatability assessment for the radiographic measurements. Hence, a future investigation that calculates intra- and interobserver variability is necessary. In addition, the study did not investigate the relationship between clinical symptoms and radiographic findings associated with dysplastic coxofemoral joints. The reason is that our study focused solely on the morphometric criteria and radiographic measurements of normal, near normal, and dysplastic coxofemoral joints (ie, modified-FCI scoring). Besides, the clinical signs of CHD do not always correlate with the degree of radiological alterations associated with diseased joints.41 The lack of hip joint laxity assessment using distraction index measurement (PennHip DI) may limit the usefulness of our radiographic determination of AFH coverage, as the examination of joint laxity is expected to exclude more individuals from the breeding pool.20 Therefore, a future radiographic and clinical study investigating German Shepherd Dogs and other dog breeds with and without hip dysplasia is warranted.

Conclusions

Norberg and CE angles below 103° and 20.8°, respectively, suggest a lack of optimum lateral AFH coverage and thus joint incongruence. To assess lateral AFH coverage of each joint independently, the CE angle is more useful than the NA. Dorsal AFH coverage width and area indexes < 49% and 51%, respectively, suggest a lack of optimum dorsal AFH coverage and thus joint incongruence. Despite the strong correlation between the measures utilized to assess lateral and dorsal AFH coverage, the authors still recommend considering both assessments when evaluating the overall AFH coverage during screening. A steep cranial acetabular edge and coxa vara are consistent with severely dysplastic coxofemoral joints. Ideally, German Shepherd Dogs with perfectly normal coxofemoral joints should be included in breeding strategies. However, to avoid the expected possibility of breed extinction over generations, including both normal and near normal joints is suggested by the authors of the present study. Our proposed FCI scoring system may achieve long-term improvement in the German Shepherd Dogs’ offspring via selective breeding of parents with phenotypically normal coxofemoral joints; however, a follow-up investigation is still required to confirm this possible improvement.

Supplementary Materials

Supplementary materials are posted online at the journal website: avmajournals.avma.org

Acknowledgments

The authors declare no competing financial interests, and none of the authors have any conflict of interest or relation with a third party that may bias the publication of this report.

The data sets supporting our results are included in the article. Raw data are available upon official request to Dr. Mostafa (aymostafa@cu.edu.eg).

Ethical review and approval were not needed as the retrospective nature of the current study relied solely on the medical records reviews and radiographic images that were routinely generated during the veterinary care of our enrolled dogs.

The authors acknowledge the technicians and radiology services for their assistance with data collection.

All authors provided the original conception of the project and participated in the research design. AAM and MAN developed the measurement techniques, approved the selected radiographs, performed data collection and analysis, and drafted the manuscript. CRB supervised and approved all aspects of the research, reviewed the manuscript, and gave the final approval for the manuscript to be published.

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