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Original Research 445

Comparison of Early Measurements of the Distraction


Index, Norberg Angle on Distracted View and the
Official Radiographic Evaluation of the Hips of
215 Dogs from Two Guide Dog Training Schools
Mathieu Taroni1,2 Jean-Pierre Genevois1,2 Eric Viguier1,2 Paul Pillard1,2 Véronique Livet1,2
Thibaut Cachon1,2 Claude Carozzo1,2

1 Department of Small Animal Surgery, Campus Vétérinaire de Lyon, Address for correspondence Jean-Pierre Genevois, DVM, PhD,
Marcy L’Etoile, France Department of Small Animal Surgery, Campus Vétérinaire de Lyon,
2 Unite ICE UPSP 2011-03-101, VetArgo Sup, Campus Vétérinaire de 69280, Marcy l’Etoile, France (e-mail: jp.genevois@free.fr).
Lyon, Marcy-l’étoile, France

Vet Comp Orthop Traumatol 2018;31:445–451.

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Abstract Objectives The main purpose of this article is to evaluate the correlation between the
distraction index (DI) and Norberg angle values in distracted hips (distraction Norberg
angle, DNA) at 4 months of age and the official hip score based on the Fédération
Cynologique Internationale (FCI) grid at 12 months of age.
Methods For dogs (n ¼ 215) from two guide dog training organizations, the DI and
DNA were measured by a single expert on distraction radiographs performed at
4 months of age. The FCI score was determined by the same expert at 12 months of age
on a standard hip-extended view.
Statistical analysis included receiver operating characteristic curve analysis and con-
cordance correlation coefficient calculation.
Results The mean DI was 0.48, the mean DNA was 86.5° and 59.5% of hips had an A
FCI score. The concordance correlation coefficient of DI and DNA was 0.78. The DI
threshold for D- and E-scored hips that was associated with the least misclassification
was 0.58 (sensitivity [Se] ¼ 0.6, specificity [Sp] ¼ 0.82). The DNA threshold that was
Keywords associated with the least misclassification was 85° (Se ¼ 0.83, Sp ¼ 0.68).
► hip dysplasia Clinical Significance DNA has a fair correlation with DI at 4 months and reflects hip
► distraction index passive laxity. D and E FCI scores at 12 months cannot be reliably predicted from the
► distracted Norberg 4 months value of DI or DNA but 96% of hips with DI < 0.58 at 4 months had an A, B or C
angle FCI score at 12 months of age. Similarly, 98% of hips with DNA > 85° at 4 months had an
► FCI grade A, B or C FCI score at 12 months of age.

Introduction
interact, predisposing dogs to developmental malformation
Canine hip dysplasia, first described by G. Schnelle1 in the of the hip joints. In predisposed dogs, environmental factors
1930s, is one of the most common orthopaedic conditions in modify the genetic influence, leading to anatomical anoma-
dogs, but its precise aetiology remains poorly understood. lies and clinical discomfort. Henricson and colleagues2 in
Hip dysplasia is a complex disease in which multiple genes 1966 described canine hip dysplasia as a disease that stems

received © 2018 Georg Thieme Verlag KG DOI https://doi.org/


December 27, 2017 Stuttgart · New York 10.1055/s-0038-1668087.
accepted after revision ISSN 0932-0814.
June 9, 2018
446 Comparison of Distraction Index and FCI Evaluation Taroni et al.

from ‘a varying degree of hip laxity of the hip joint permitting 24 months of age or older. Concerns regarding earlier diag-
subluxation during early life, giving rise to varying degrees of nosis explain the growing interest in distraction radiographs
shallow acetabulum and flattening of the femoral head, in the veterinary literature in the last few decades.
finally inevitably leading to osteoarthritis’. Distraction methods as described by the PennHip orga-
Hip dysplasia is a concern in pet dogs but also and nization14–16 have been shown to be reliable screening
particularly in working dogs. Guide dog training organiza- methods to predict hip dysplasia as early as 16 weeks of
tions, for instance, attempt to foresee the evolution of the age.13,17,18 Norberg angle measurement with the femur in a
dogs enrolled in their training programme by subjecting neutral position and hips distracted (distraction Norberg
their breeding dogs to hip radiographic screening and apply- angle, DNA) was first described by Adams and colleagues.13
ing selection pressure in an attempt to maximize the Compared with the regular Norberg angle measured on the
improvement in hip joint quality in the offspring. In spite hip-extended radiograph, DNA is free from the coxofemoral
of these preventive measures, emphasizing the importance joint capsule windup19 that limits the lateral movement of
of screening organizations all around the world, mating dogs the femoral head. Very few studies report the use of
with normal hips, even with normally conformed ancestors, DNA,13,20 but it may be hypothesized that DNA can be as
does not produce all normal offspring.3–10 reliable as the distraction index (DI) for hip laxity
Screening of breeding dogs as well as pet or working dogs measurement.
is based on radiographic evaluation. A standard hip- The purpose of this study is to evaluate the correlation
extended radiograph, in anaesthetized or deeply sedated between DI and DNA measured at 4 months of age and the FCI
dogs, is mostly used for official hip radiographic screening. official hip score determined at 12 months of age.

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The Fédération Cynologique Internationale (FCI) system is
used in continental Europe, Asia, Russia and parts of South
Materials and Methods
America. It is based on a five-grade (A, B, C, D, E) scoring scale
from A, reflecting a normal hip joint, to E, indicating severe Data Collection
hip dysplasia. Assessment criteria include the value of the Radiographic data from dogs (n ¼ 215) from two guide dog
Norberg angle, degree of subluxation, shape and depth of the training organizations were collected from one author’s
acetabulum and signs of secondary joint disease.11 database (JPG). Dogs had been line-bred for favourable
Hip dysplasia screening tests should minimize false-nega- characteristics, including hip conformation. The population
tive diagnoses. For working dogs, it is of upmost interest to included mainly Labrador and Golden Retrievers and other
rule out from an expensive training programme the indivi- miscellaneous breeds (German Shepherd, Labrador/Golden
duals which are most likely to develop osteoarthritis. Hip- cross breed, Labrador/Poodle cross breed, Golden/German
extended radiographic screening is not considered as accu- Shepherd cross breed). Radiographs were performed
rate before 12 months of age at least.12,13 Therefore, FCI between January 2013 and December 2016.
regulation states that the minimal age for official hip grading At 4 months of age, dogs underwent stress radiographs
is 1 year for most breeds and 18 months for large and giant using the technique described by Vezzoni and colleagues.21
breeds. The Orthopedic Foundation for Animals requires After a first standard hip-extended radiograph, a ventrodor-
official hip radiographs to be performed on dogs that are sal compression view was performed, followed by a

Fig. 1 Box and whisker plots of the distraction index in the total population and in the three most represented breeds.

Veterinary and Comparative Orthopaedics and Traumatology Vol. 31 No. 6/2018


Comparison of Distraction Index and FCI Evaluation Taroni et al. 447

Fig. 2 Box and whisker plots of the distraction Norberg angle in the total population and in the three most represented breeds.

Downloaded by: The University of Edinburgh. Copyrighted material.


distraction view using a Vezzoni distractor. At 12 months, a Statistical Analysis
standard ventrodorsal hip-extended radiograph was per- Each hip was evaluated as an independent joint, regardless of
formed to obtain an official FCI scoring. The radiographs the other hip of the dog.
were performed on anesthetized dogs in five different veter- The normal distribution of numeric variables was tested
inary practices by five different well-trained veterinarians. with the Shapiro–Wilk test. The mean and median DI and
The digital DICOM radiographs were sent to one of the DNA were calculated successively for the whole population,
authors for measurement and evaluation via a dedicated for the Labrador Retriever population, for the Golden Retrie-
computerized programme (EasyIMAGE—VetXL, VetZ, Han- ver population and for each of the 5 FCI score categories
over, Germany). among the total population of dogs.
The FCI class was grouped as follows: hips graded A, B, C
Hip Evaluation were considered clinically acceptable and hips graded D, E
The DI and DNA were assessed on both hips for all the dogs on were considered as non-acceptable.22
the 4 months radiographs. The FCI official grading from A to E The threshold analysis of the DI and the DNA was per-
was performed by the same expert based on the 12 months formed with a receiver operating characteristic (ROC) curve
hip-extended radiographs. analysis.23

Fig. 3 Distraction index among Fédération Cynologique Internationale categories.

Veterinary and Comparative Orthopaedics and Traumatology Vol. 31 No. 6/2018


448 Comparison of Distraction Index and FCI Evaluation Taroni et al.

Fig. 4 Distraction Norberg angle among Fédération Cynologique Internationale categories.

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The DNA and DI values were centred and scaled. The weeks old, and the mean age for the 12-month evaluation
correlation between the centred-scaled variables was eval- was 54.3  1.8 weeks.
uated with Lin’s concordance correlation coefficient The DI was not normally distributed (p ¼ 0.004) and the
(CCC).24,25 The CCC is composed of a measure of precision DNA did not significantly diverge from normality (p ¼ 0.06).
rho and accuracy C.b. The CCC ranges from 0 to 1, 1 being a The median value of the DI was 0.47 (range values 0.17–0.92)
perfect agreement between measurement methods. (►Fig. 1). The median value of the DNA was 86° (range values
The analysis was performed using R 3.4.0 (R Foundation 68°–105°) (►Fig. 2). Repartition of the FCI scores was 59.5%
for Statistical Computing, Vienna, Austria) and the package (n ¼ 256) A (no sign of hip dysplasia), 21.9% (n ¼ 94) B (near
pROC. A value of p < 0.05 was considered significant. normal hip joint), 11.2% (n ¼ 49) C (mild hip dysplasia), 4.0%
(n ¼ 17) D (moderate hip dysplasia) and 3.5% (n ¼ 15) E
(severe hip dysplasia). The repartition of the DI values and
Results
the DNA values among the FCI categories are represented in
In the total population, 167 dogs were Labrador Retrievers, ►Figs. 3 and 4, respectively.
26 were Golden Retrievers, 8 were German Shepherds, 5 The difference between the ROC curves of DI and DNA was
were Labrador/Golden cross breed, 1 was a Labrador/Poodle not significant (Bootstrap test for correlated curves, p ¼ 0.27).
cross breed and 8 were Golden/German Shepherd cross For the DI and DNA, the CCC was 0.78. The precision and
breeds. Among them, 82 were males, 133 were females. accuracy were rho ¼ 0.78 and C.b ¼ 0.9999983, respectively.
The mean age for the 4-month evaluation was 16.7  0.7 The two methods were on average centred on the same

Table 1 Variation in specificity, sensitivity, positive predictive value and negative predictive value depending on the threshold of
distraction index chosen, for a prevalence of hips graded E or F of 7.42%

Thresholds Specificity Sensitivity Positive predictive value Negative predictive value


0.1 0.0056 1.00 0.0748 1.00
0.2 0.0168 1.00 0.0755 1.00
0.3 0.0702 0.9667 0.0771 0.9632
0.4 0.2865 0.9333 0.0951 0.9816
0.5 0.6152 0.7333 0.1328 0.9663
0.58 0.8146 0.6 0.2064 0.9620
0.6 0.8343 0.5 0.1952 0.9540
0.7 0.9522 0.2333 0.2818 0.9391
0.8 0.9944 0.1 0.5894 0.9321
0.9 1 0.0333 1.00 0.9278

Veterinary and Comparative Orthopaedics and Traumatology Vol. 31 No. 6/2018


Comparison of Distraction Index and FCI Evaluation Taroni et al. 449

The DNA threshold that was associated with the least


misclassification was 85° (Se ¼ 0.83, Sp ¼ 0.68) (►Table 2).
The ROC curve is represented in ►Fig. 6.

Discussion
Our results showed that the DI and DNA measured at
4 months of age cannot accurately predict the FCI score at
12 months of age. A fair correlation between DNA and DI
values at 4 months was found.
In the past, it has been questioned whether hip laxity can
be properly assessed on hip-extended radiographs. It is not
Fig. 5 Receiver operating characteristic curve of the ability of the
considered accurate until the age of 12 months for the
distraction index to discriminate A, B and C Fédération Cynologique
Internationale (FCI) grade from E and F FCI grades. The black curve diagnosis of hip dysplasia. At 6 months of age, only 16 to
indicates the evolution of the specificity and the sensitivity when the 32% of dogs with hip dysplasia are correctly diagnosed, and at
threshold is modified. The grey line represents a non-informative 1 year of age, correct diagnosis is reported for 63 to 69% of
index. The closer the black line to the point (1.1) on the top left corner, dogs.12,13 On the other hand, several studies have shown that
the better the performances of the test. The area under the curve is
early DI measurement on a distraction radiograph with the
0.7571.
limbs in a neutral position is a good indicator of passive hip

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laxity and thus a good predictor of canine hip dysplasia in
values with an almost perfect accuracy. The variation in terms of osteoarthritis development after 2 years of age or
measurements was more important but still gave a fair pre- later in the dog’s life.17,26,27 Among the hips which had a FCI
cision. As a result, the CCC gave an overall fair agreement score of A, only 6.2% had a DI 0.3 and 3.1% had DI > 0.7. This
between DI and DNA. underlines the fact presented above whereby FCI scoring
The DI threshold that was associated with the least based on hip-extended radiographs is not accurately related
misclassification was 0.58 (Se ¼0.6, Sp ¼ 0.82) (►Table 1). to passive laxity. The DI threshold associated with the
The ROC curve is represented in the ►Fig. 5. least misclassification is 0.58 and its associated negative

Table 2 Variation in specificity, sensitivity, positive predictive value and negative predictive value depending on the threshold of
DNA chosen, for a prevalence of hips graded E or F of 7.42%

DNA Thresholds Specificity Sensitivity Positive predictive value Negative predictive value
105 0.0084 1 0.0750 1
103 0.0113 1 0.0752 1
101 0.0226 1 0.0760 1
99 0.0254 1 0.0762 1
97 0.0621 1 0.0789 1
95 0.1356 0.9667 0.0824 0.9806
93 0.2373 0.9667 0.0924 0.9888
91 0.3220 0.9667 0.1028 0.9917
89 0.4633 0.9333 0.1226 0.9885
87 0.5706 0.8667 0.139 0.9815
85 0.6780 0.8333 0.1722 0.9806
83 0.7853 0.6 0.1834 0.9606
81 0.8644 0.4667 0.2167 0.9527
79 0.9350 0.3 0.2706 0.9432
77 0.9520 0.1667 0.2182 0.9343
75 0.9831 0.1667 0.4422 0.9362
73 0.9887 0.1333 0.4867 0.9342
71 0.9944 0.0666 0.4890 0.9298
69 1 0.0333 1 0.9279

Abbreviation: DNA, distraction Norberg angle.

Veterinary and Comparative Orthopaedics and Traumatology Vol. 31 No. 6/2018


450 Comparison of Distraction Index and FCI Evaluation Taroni et al.

ability of the DI measurement has been reported by the


PennHIP organization,32 it might not be the case for the DNA
measurement at 4 months, that is, before the ossification of
the craniolateral edge of the acetabulum. This might have
diminished the importance of the correlation.
In conclusion, DNA is correlated with DI in 4-month-old
dogs. The DNA may be an interesting indicator and should
undergo further consideration to determine if it can offer
complementary information to refine early hip laxity eva-
luation. The FCI grades at the age of 12 months have a poor
correlation with DI and DNA, but our results suggest that a
threshold of 0.58 for the DI or 85° for the DNA at 4 months
Fig. 6 Receiver operating characteristic curve of the ability of the
can accurately predict A, B or C-scored hips at 12 months.
distraction Norberg angle to discriminate A, B and C Fédération
Cynologique Internationale (FCI) grade from E and F FCI grades. The
black curve indicates the evolution of the specificity and the sensi- Funding
tivity when the threshold is modified. The grey line represents a non- This research did not receive any specific grant from
informative index. The closer the black line to the point (1.1) on the funding agencies in the public, commercial or not-for-
top left corner, the better the performances of the test. The area
profit sectors.
under the curve is 0.7885.

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Conflict of Interest
predictive value is 0.96. This means that 96% of dogs with a None.
DI < 0.58 have an A, B or C FCI score. These results must be
interpreted with caution due to the overrepresentation of A- Author Contributions
scored hips, the poor representation of E-scored hips in our All authors contributed to conception of study, study
population and the poor correlation found between the DI design, and acquisition of data and data analysis and
and FCI score. The PennHIP method and thus the DI mea- interpretation. All authors drafted, revised and approved
surement have been reported as accurate to predict FCI the submitted manuscript.
scores D and E.28 Our study does not confirm these results
but the poor representation of D and E hips in our population Acknowledgment
is a bias for the interpretation of our results regarding this The authors acknowledge the two schools of guide dogs
category of hips. Indeed, 33.3% of hips with a DI > 0.7 had an for blind people and the veterinarians collaborating with
FCI score of A, and 19.1% had an E FCI score. It seems peculiar these schools, who performed the radiographs.
to claim that dogs with a DI > 0.7 are more likely to have A-
scored hips than E-scored hips.
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