Canine hip dysplasia is the most commonly inherited orthopedic disease in dogs. Described by Schnelle in 19351 as a malformation of the hip joint, it has since been recognized as the primary orthopedic disease affecting medium- to large-breed dogs.2–4 Canine hip dysplasia is expressed by a shallow acetabulum, subluxation of the femoral head, changes in the shape of the femoral head or neck, or periarticular osteophytes5 and can be influenced by environmental factors.6,7 Canine hip dysplasia is a polygenic and multifactorial disease that is highly heritable.4,8–10 Studies5,9–14 have shown, in various populations and breeds, that CHD heritability estimates range from 0.10 to 0.60.
Riser15 stated that maintaining stability and congruency in the hip joint could prevent CHD in young dogs. Hip joint laxity is an early sign of CHD,16 and primary joint laxity causes the changes in the acetabulum.11 Degenerative joint disease occurs when the femoral acetabulum contact is altered, resulting in an abnormal position of the femoral head and acetabulum and causing instability.15 Environmental factors, age, breed, body weight, frame size, strenuous activity, or poor muscle mass influence hip joint laxity.5–7,11,17,18 Degenerative joint disease occurs when passive hip joint laxity converts to weight-bearing laxity.7
The OFA provides a subjective hip joint quality scoring method that has been used as a diagnostic tool since 19663 and is the most prevalent hip joint measurement tool used in the world.16,19 A 7-point grading scale is used to describe hip quality from ventrodorsal hip joint–extended pelvic radiographs. On radiographic evaluation, nondysplastic hip joints are classified as excellent, good, or fair, and dysplastic hip joints are classified as mild, moderate, or severe. Hip joints are classified as borderline if no arthritic changes are present but they have more incongruity than in hip joints classified as fair. Subjective measures are best used in dogs ≥ 24 months of age. The false-negative rate of evaluation is much higher in dogs < 24 months of age.20 In the last 4 decades, Labrador Retriever OFA hip joint scores have shown variable improvements in hip joint quality, but the overall proportion of hip joints classified as excellent has increased by 24%. The overall proportion of hip joints classified as excellent increased in 2000 to 2007 from 22% to 27%.13
The PennHIP evaluation measures passive hip joint laxity from radiographic views of the pelvis under stress (ie, compression and distraction views).7 When a distraction force is applied to the pelvis, the femoral head displaces from the center of the acetabulum by a measurable distance that is divided by the radius of the femoral head, which yields a unitless measure of joint laxity.7 Scores range from 0 to 1 (or more), with 0 considered as having no laxity and 1 considered as severe laxity. Distraction index values have been shown to be more accurately predictive of the risk of developing DJD than subjective hip joint scoring methods for dogs < 24 months of age.7,18
Working dogs in canine detection programs protect against current and emerging threats, and the demand for specialized detection dogs has increased.21,22 Otherwise successful detection dogs are rejected from service because of poor hip joint quality ratings. Evans et al23 found DJD to be one of the primary reasons for discharge of Department of Defense military working dogs ≥ 5 years of age. Reducing and eliminating CHD through selective breeding are imperative for improving the functionality and working longevity of detection dogs. To reduce CHD in a population, pedigree depth should be established and only dogs with nondysplastic hip joints should be mated.8 Breeding programs should examine phenotypic expressions of CHD across several generations when making sire and dam selections.4,16 The purpose of the study reported here was to examine the effectiveness of applying selective pressure to improve hip joint quality in a purpose-bred detection dog population by use of the PennHIP DI value along with the OFA hip joint quality rating system and to determine whether age, sex, coat color, breed, and body weight were associated with hip joint quality.
Materials and Methods
Animals
Orthopedic records of 615 dogs (315 males, 300 females) from the Auburn University College of Veterinary Medicine-Canine Performance Sciences breeding program between 2000 and 2017 were analyzed. The population consisted of Labrador Retrievers (n = 569) from 102 litters from 43 dams and 47 sires, and Labrador Retriever–German Wirehaired Pointer crossbred dogs (46) from 8 litters of F1, F2, and F3 generations from 6 dams and 6 sires. Seven dogs were removed from the 2015 to 2017 analysis because they had undergone only 1, not both OFA and PennHIP evaluations.
Dogs were presented to the Bailey Small Animal Teaching Hospital at the Auburn University College of Veterinary Medicine for routine hip joint radiographic evaluation. Radiography was not conducted if females were in estrus. Dogs were sedated, and standard ventrodorsal hip joint–extended and stress (ie, compression and distraction) radiographic views of the pelvis were obtained and submitted for OFA and PennHIP evaluations, accordingly. PennHIP-certified veterinarians (JH and RL) participated in obtaining the radiographic views. The worst-rated hip joint without regard to hip joint of origin (ie, left or right) as indicated by OFA hip joint score or DI value was selected for use in statistical analysis. For the purpose of statistical analysis, dogs were grouped into fiscal year contemporary groups on the basis of their birth date. The fiscal year spanned from October 1 to September 30 (eg, a dog born in December 2000 would be in the fiscal year 2001 group).
Prior to 2015, the only hip joint requirements for breeding stock were to have excellent or good OFA hip joint scores. Since 2015, hip joint requirements for matriculation as breeding stock were a DI value of ≤ 0.30 and an OFA hip joint score of excellent or good. Dogs with excellent or good OFA hip joint scores and DI slightly > 0.30 were infrequently permitted as breeding stock because of their other outstanding behavioral phenotypes. Successful detection dogs must possess certain behavioral characteristics, such as the ability to hunt, focus, and work independently.24 After all breeding stock medical requirements were satisfied (eg, free of CHD), mating selections were based on inbreeding coefficients, management of other genetic traits (eg, exercise-induced collapse), and behavioral characteristics.
Dog care and use activities were approved and monitored by the Auburn University Institutional Animal Care and Use Committee.
Statistical analysis
Commercially available softwarea was used for data analysis. To assess whether hip joint quality scores improved over time, the Kendall rank (τ) and Spearman rank-order (r) correlations were run to determine relationships between OFA hip joint score and fiscal year (before and after implementing PennHIP evaluation as a selective breeding technique) and DI value and fiscal year, respectively. A Pearson c2 test of homogeneity was used to analyze the effectiveness of the use of DI values in improving OFA hip joint scores. Dogs missing either measurement (ie, DI value or OFA hip joint score) were removed from the analysis. A Spearman rank-order correlation was determined to assess the relationship between OFA and DI screening methods for detecting evidence of CHD. Multiple regression analysis was used to evaluate age, sex, coat color, breed, and body weight as predictors of DI value. A Pearson c2 test was performed to evaluate the association of sex with OFA hip joint score. For all tests, values of P ≤ 0.05 were considered significant.
Genetic softwareb was used for heritability analysis. Four measures of hip joint scores based on the DI values were used for this analysis as follows: right hip joint score, left hip joint score, mean hip joint score (average value of right and left hip joint scores), and final hip joint score (maximum value of the right and the left hip joint scores). A quantitative trait maximum likelihood model with sex as a covariate was used. Values of P < 0.05 were considered significant.
Results
From 2001 through 2014, 429 dogs were assessed by OFA evaluation only. From 2015 through 2017, 179 dogs were assessed by both OFA and DI screening methods for detecting evidence of CHD. Seven dogs were removed from the 2015 through 2017 analysis because they had undergone only 1 but not both OFA and PennHIP evaluations.
The mean ± SD age of dogs that were evaluated was 10.85 ± 1.27 months. The mean ± SD body weight of evaluated dogs was 27.35 ± 3.62 kg (60.17 ± 7.96 lb). Since 2015, Labrador Retriever sires and dams (n = 16) had a mean ± SD DI value of 0.37 ± 0.10 and Labrador Retriever–German Wirehaired Pointer crossbred sires and dams (3) had a mean ± SD DI value of 0.38 ± 0.08.
From 2001 through 2014, the correlation between OFA hip joint scores and year (ie, before the implementation of PennHIP evaluation) was not significant (τ = −0.044; P = 0.242). From 2015 through 2017, the correlation between OFA hip joint scores of dogs and year (ie, during which time the PennHIP evaluation was used in combination with OFA evaluation) was significant (positive correlation, τ = 0.249; P < 0.001). The decrease in DI values across years was not significant (r = −1.06; P = 0.156).
Of dogs assessed by only OFA evaluation from 2001 through 2014, 75% (323/429) had nondysplastic hip joints (ie, OFA hip joint scores of excellent, good, or fair) and 16% (68/429) had dysplastic hip joints (ie, OFA hip joint scores of mild, moderate, or severe). Nine percent (38/429) of dogs had borderline hip joints on the basis of OFA evaluation. After implementing selective breeding with the incorporation of PennHIP evaluation, the percentage of dogs with nondysplastic hip joints increased by 22 percentage points to 97% (181/186), whereas 3% (5/186) of dogs had dysplastic hip joints and none had borderline hip joints (Figure 1). The decrease in the percentage of dogs with dysplastic hip joints after the introduction of DI values was significant (P < 0.001). The mean DI value for the entire population was 0.38 ± 0.10. A significant (r = −0.279; P < 0.001) negative correlation was found between DI and OFA screening methods for detecting evidence of CHD; as OFA scores improved, DI values decreased.
Results of multiple regression analysis that included age, sex (male vs female), coat color (black, yellow, or chocolate), breed (Labrador Retriever vs Labrador Retriever–German Wirehaired Pointer crossbred dogs), and body weight as predictors of DI values indicated that only sex and age were significant (P < 0.001) predictors of the DI value. An increase in age was associated with a decrease in the DI value, and dogs closer to 11 months of age had less hip joint laxity than younger dogs. Sex was a significant predictor of DI values, and female was associated with an increase in DI values. Hip joint scores obtained by OFA standards did not, however, differ (P = 0.614) by sex.
Heritability analysis of OFA hip joint scores for 189 dogs revealed that the total additive genetic heritability score was 0.18 to 0.26 for all 4 hip joint score phenotypes, and all heritability scores were significantly (ie, P < 0.05) > 0. In all models fitted for the 4 CHD heritability scores, the effect of sex was not significant.
Discussion
The demand of specialized dogs for the detection of hazardous materials and emerging threats has steadily increased during the last several years.21,22 Degenerative joint disease, the phenotypic expression of CHD, is one of the primary reasons for release of military working dogs ≥ 5 years of age.23 In 2007, Evans et al23 found that 42 of 160 military working dogs were discharged from service because of DJD alone or DJD in conjunction with spinal cord disease. Reducing and eliminating CHD through selective breeding could improve the functionality and working longevity of detection dogs. In the study reported here, we examined the effectiveness of applying selective pressure with PennHIP DI values along with hip joint scores obtained by OFA standards to reduce the prevalence of CHD in a population of purpose-bred detection dogs.
In the present study, the addition of DI values as a selection tool for breeding animals significantly improved the OFA hip joint scores of the population from 2015 through 2017. Dogs deemed to have tight (nonlax) hip joints when screened by use of objective measures (ie, DI value < 30) have minimal risk of developing CHD.7,18 In contrast, following the subjective OFA guidelines by only breeding dogs with hip joint confirmation classified as excellent or good, no significant progress had been made in our population during the course of 13 years. Historically, subjective scoring methods, such as OFA evaluation, have produced measurable effects on breeding populations.13 However, researchers have recently found that excess joint laxity, as seen by radiographic views included in PennHIP evaluation, was not always apparent on the standard hip joint–extended pelvic radiographs used by subjective scoring methods, allowing dogs with greater hip laxity to be inaccurately judged as having good-quality hip joints.7,25 Dogs with even good subjective hip joint quality scores may produce affected offspring.5,25
The addition of DI values to hip joint scores obtained by OFA standards created a stronger individual phenotype grade for hip joints. Use of the OFA guidelines was successful in removing dogs most at risk for CHD from our population; however, the addition of DI values as a breeding selection tool substantially accelerated the progress. The use of DI values significantly improved our population's OFA hip joint scores by 22 percentage points during a 3-year period, which supports the findings from the 1977 study of Leighton,16 who found a significant decrease in CHD in a population of Labrador Retrievers and German Shepherd Dogs by using a combination of DI values and subjective radiographic scores to determine breeding stock replacements.
Studies4,5 have reported CHD occurring more frequently in female dogs, but most studies4,12,13,17,26–29 found no sex predilection. Sex was not a significant factor for the prevalence of CHD in our population, which agreed with the results of other studies12,13; however, sex and age were significant predictors of DI value in our population. Female dogs in our population had significantly more laxity in their hips than male dogs, which supports the findings of Ginja et al19 from a population of Estrela Mountain Dogs. This difference could be attributed to the hormonal difference in males and females. One study30 found puppies that ingested increased amounts of immunoactive relaxin, estrogen, and estrogen precursor concentrates via their dam's milk were found to have increased hip joint laxity later in life. Dogs in our population closer to 11 months of age had less hip laxity than younger dogs; however, had the number of older dogs included increased, we may expect a parabolic function because DJD disease susceptibility increases with age.18
The use of selective breeding in our population of dogs resulted in an increased prevalence of hip joints classified as good by OFA standards and a decreased prevalence of hip joints classified as mild, moderate, and severe by OFA standards; these findings supported the theory that CHD is a polygenic trait.4,8,9 Heritability of OFA hip joint score in our population ranged from 0.18 to 0.26, indicating that CHD is a mildly heritable trait. Other studies reported similar heritability of CHD ranging from 0.22 to 0.30 in various dog breeds,12,31 whereas in a recent study,14 the heritability analysis of CHD in Labrador Retrievers revealed a higher rate of 0.59. Variances in heritability may be caused by the various breeds studied, evaluation of hip joint phenotype, method used for heritability calculation, or sample sizes. Sex was not a significant factor for the presence of CHD in our population, which agreed with the results of other studies.12,13
The use of estimated breeding values has been shown to be effective in reducing CHD in populations of dogs.16,32 Estimated breeding values calculate a dog's genetic risk for developing specific conditions by use of pedigree relationships along with heritability estimates.16 Zhang et al33 suggested using a joint estimated breeding value from DI values, dorsolateral subluxation measurements, Norberg angles, and hip joint–extended radiographic measures to decrease CHD in breeding populations.33
Organizations in the United States have developed estimated breeding value analyses for breeders to access free online, based on publicly registered OFA scores. Although databases like these may continue to help eliminate dogs most at risk for CHD from the overall population, it may not substantially reduce CHD in breeding populations in a timely manner.13 One challenge in accessing estimated breeding values with only the use of OFA hip joint scores is that not all progeny are included. From 1970 to 2000, only dogs with hip joint scores classified as excellent, good, and fair by OFA standards were publicly reported.13 Breeding animals examined by use of subjective scores alone may produce affected offspring.5,25 When estimating breeding values to improve OFA hip joint scores, the population's hip joint heritability estimates must be understood,16 and for breeders without complete pedigree evaluation or access to that level of management, the addition of PennHIP evaluation for sire and dam selection to reduce CHD is appropriate and cost-effective. To make progress in reducing CHD in a breeding population, breeders should determine their population mean DI value and select breeding stock that has a DI value that is lower than their population mean DI value. Worth et al34 and Ginja et al35 found that PennHIP evaluation was the best method for making greater gains over fewer generations in German Shepherd Dogs and Estrela Mountain Dogs, respectively, which supports our findings presented here.
Dogs leave our population to begin work around 12 months of age; therefore, documenting that dogs were negative for CHD at 24 months of age was not possible. Further, because of the retrospective and correlational nature of this study, we cannot conclusively claim a causal effect of DI values on OFA hip joint scores. Through selective breeding validated by OFA and PennHIP evaluations, however, our population has been free from CHD since the fiscal year of 2015.
Regardless of these limitations, our data suggested that PennHIP evaluation is effective at reducing the prevalence of CHD in a breeding population. Our findings indicated that DI values should be used when selecting breeding stock as it produces a quantifiable value and has been shown to significantly improve OFA hip joint scores in a population of purpose-bred working dogs.
Acknowledgments
Supported by the Auburn University College of Veterinary Medicine-Canine Performance Sciences Donors and the Help Raise a Hero Fund.
Dr. Xu Wang was supported by a laboratory start-up fund from Auburn University College of Veterinary Medicine and the USDA National Institute of Food and Agriculture, Hatch project No. 1018100.
The authors declare that there were no conflicts of interest.
The authors thank Dr. Eldin Leighton for providing leadership and technical assistance.
ABBREVIATIONS
CHD | Canine hip dysplasia |
DI | Distraction index |
DJD | Degenerative joint disease |
OFA | Orthopedic Foundation for Animals |
Footnotes
SPSS, version 25.0 for Windows, SPSS Inc, Chicago, Ill.
SOLAR-Eclipse genetic software, University of Maryland, Catonsville, Md. Available at: solar-eclipse-genetics.org/. Accessed Feb 5, 2019.
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