Canine heupdysplasie screening: vergelijking van vroege evaluatie met definitieve beoordeling bij 231 honden met Fédération Cynologique Internationale A en B

Canine heupdysplasie screening: vergelijking van vroege evaluatie met definitieve beoordeling bij 231 honden met Fédération Cynologique Internationale A en B

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Open Access

Peer-reviewed

Research Article

  • Roxana Merca, 
  • Barbara Bockstahler, 
  • Aldo Vezzoni, 
  • Alexander Tichy, 
  • Simona Boano, 
  • Britta Vidoni
PLOS

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Abstract

Objectives

This study aimed to verify if a significant difference exists between parameters in the early evaluation of normal and near-normal hip joints, to evaluate the influence of age and breed on the parameters, and to clarify the usefulness of a total score for differentiating between Fédération Cynologique Internationale (FCI) grade A and B hips.

Methods

A total of 231 dogs were classified according to whether they had FCI A or B hips at adulthood, with measurements obtained at 14–28 weeks of age. The total score was calculated by the summation of the following quantitative parameters: angle of subluxation (AS), angle of reduction (AR), laxity index (LI), and dorsal acetabular rim slope (DARS). Logistic regression analysis was performed to establish the probability of the study population to develop an FCI B hip based on the total score. This was repeated for the highest score in combination with the worst-rated hip and once more for breeds.

Results

No correlation between age and the parameters was found in the cohort, or for FCI A and B. The values of all the parameters were significantly lower in the FCI A group than in the FCI B group (AR: 4.42° ± 6.0° vs 7.62° ± 7.2°; AS: 0.45° ± 1.9° vs 1.55° ± 3.8°; LI: 0.32 ± 0.1 vs 0.36 ± 0.1; DARS: 3.30° ± 1.8° vs 3.77° ± 1.9°; TS: 11.47 ± 8.3 vs 16.65 ± 10.9). Labrador Retrievers and Golden Retrievers showed significant differences between parameters for both FCI grades. The range, where FCI A and B hips can be predicted on the basis of the total score, was different when assessed for the entire cohort, Labrador Retrievers, and Golden Retrievers.

Clinical significance

Our results show that even in normal and near-normal hips, the parameters significantly differed in the early evaluation. Moreover, cutoff values should be set for different breeds in the prediction of the FCI grade during early evaluation for a better breeding selection regarding canine hip dysplasia, one of the most common orthopedic diseases among large and giant breed dogs.

Citation: Merca R, Bockstahler B, Vezzoni A, Tichy A, Boano S, Vidoni B (2020) Canine hip dysplasia screening: Comparison of early evaluation to final grading in 231 dogs with Fédération Cynologique Internationale A and B. PLoS ONE 15(5): e0233257. https://doi.org/10.1371/journal.pone.0233257

Editor: Silvia Sabattini, University of Bologna, ITALY

Received: May 19, 2019; Accepted: May 2, 2020; Published: May 18, 2020

Copyright: © 2020 Merca et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: The authors received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Canine hip dysplasia (CHD) is one of the most common non-traumatic orthopedic diseases in large and giant breed dogs [1,2]. The pathogenic process involves hip laxity, incongruence of the coxofemoral joint, synovitis, abnormal progression of endochondral ossification and development of osteoarthritis (OA) [3,4], manifesting as restricted joint mobility, pain, and lameness. Etiological roles for genetic and environmental factors have been described in the CHD literature. Some influencing factors such as physical activity, dietary factors or body weight can be readily modulated by the owner [2,59], but not other factors such as an anomalous inclination of the dorsal acetabulum or hormonal influences [913]. Physical and therapeutic interventions increase the cost of lifetime care (for both pet and working dogs) and, if unsuccessful, raise the option of euthanasia [13,14].

Although numerous CHD screening programs that allow phenotypic selection are common in breeding clubs, only moderate success has been achieved for the improvement of the incidence of CHD [1522]. The distinction between Fédération Cynologique Internationale (FCI) grade A and B hips is given by the Kennel clubs through their breeding regulations. In several breeds, dogs that have been evaluated as having FCI B hips are only allowed to pair with dogs that have been evaluated as having FCI A hips [23]. To our knowledge, no studies have specifically focused on the development of arthrosis in FCI A hips; however, Belgian shepherd dogs with borderline hip dysplasia have been shown to have altered joint kinematics [24]. Early evaluation (EE) of the hip joint remains a key clinical predictor of the outcome at the final evaluation performed upon skeletal maturity [9,1419,25]. Thus, EE enables decision making for early surgical preventive intervention in growing dogs [1,2629] or for timely exclusion from breeding or training programs. However, no evidence-based consensus has been reached about the precise method of EE, or the parameter profile or hierarchy for such decision making [30]. Furthermore, the thresholds and breed variations of the parameters for the prediction of the final FCI score remain undefined [19,31].

The objective of this retrospective study was to verify whether EE can reveal differences in the parameters, including laxity index (LI), dorsal acetabular rim slope (DARS), femoral head center (FHC), angle of subluxation (AS), and angle of reduction (AR), between hips later classified as FCI A or B. The study also evaluated the influences of age and breed on the different parameters, and verified the probability of differentiating between later FCI A and B classifications to facilitate early breeding selection and training purposes.

Materials and methods

The medical records in Clinica Veterinaria Vezzoni were searched for dogs with data obtained at 14–28 weeks of age at EE, without surgical preventive intervention for CHD, with FCI A or B hip at 12 months or older, and both hips evaluated separately. A total of 231 dogs (462 evaluated hips) were included in the study. The study population included mixed- and pure-breed dogs. For the evaluation of breed influence, the cohort was subdivided into breeds. All the groups with

Clinical and radiographic examinations were performed either by a surgery or imaging resident or by a board-certified surgeon. For all the dogs, EE was performed under deep sedation and included a quantitative evaluation of the Ortolani sign based on the measurements of AS and AR. The measurements were performed in dorsal recumbency using the Slocum Electronic Goniometer (Slocum Enterprises Inc., Eugene, OR, USA).

Radiographs were taken for the extended ventrodorsal, dorsal acetabular rim and distraction views [32]. The resulting parameters included LI [33], DARS [34] and FHC [35]. FHC was evaluated in the ventrodorsal view and classified as medial, superimposed, or lateral to the dorsal acetabular rim. DARS was obtained using the technique described by Slocum [34]. The distraction view was obtained as originally described by Badertscher [32], using the Vezzoni modified Bardertscher distension device (VMBDD) [33,36]. LI was measured in accordance with the method used by Smith and colleagues [8,33,3739]. After reaching skeletal maturity, all the dogs underwent CHD assessment in accordance with FCI standards [40],by a veterinarian with FCI board certification. CHD assessments according to FCI standards have been performed in the ventrodorsal radiographic view.

Data were evaluated using the SPSS version 24 statistical software (IBM Corp., Armonk, NY, USA). A total score (TS) was obtained, similar to the global index published before [19], represented by the sum of all quantitative parameters evaluated [AS AR (LI × 10) DARS], where the LI is multiplied by 10 to account for its value being always below 1. The FHC parameter was qualitative and could therefore not be included in the TS. Dogs that tested negative for the Ortolani sign were included in the statistical evaluation, with a value of 0 for both AR and AS.

The study population was divided into two groups (A and B) according to FCI grade. Logistic regression analysis was performed to establish the probability of development of grade B hips based on the TS. The left and right hips were evaluated separately. This was repeated for the highest score of each dog in combination with the worst-rated hip of each dog. Thus, in all the logistic regression analyses, the statistical unit was the dog. In addition, we performed these analyses for breed groups with >10 dogs. Odds ratios, including 95% confidence intervals, were calculated for the logistic regression using the highest TS of each dog.

The Student t test was used for the comparisons of AS, AR, LI, and DARS between the FCI A and B groups. A Pearson correlation analysis was performed to assess the correlation between age and the parameters. The chi-square test was used to evaluate the differences in FHC between groups A and B. The effects of group and breed on the different parameters were analyzed using a general linear model with the Tukey alpha correction procedure as a post hoc test for breed. The assumption of normal distribution was assessed using the Kolmogorov-Smirnov test. A p value of

Results

Demographics

The female-to-male ratio was 1:1 (50.6% females and 49.4% males). The mean age was 20.7 ± 3.4 weeks at EE and 64.3 ± 20.6 weeks at final FCI examination, with 303 FCI A and 159 FCI B hip joints. The most frequently represented breeds were Labrador Retriever (n = 93, 40.3%), Border Collie (n = 36, 15.6%), Golden Retriever (n = 36, 15.6%), and Bernese Mountain Dog (n = 31, 13.4%). A total of 216 hips tested positive for the Ortolani sign, with AR ranging from 5° to 30°. The values (mean ± SD) of the parameters in the entire study population were as follows: AR, 5.52° ± 6.6°; AS, 0.83° ± 2.7°; LI, 0.33 ± 0.1; DARS, 3.46° ± 1.8°; and TS, 13.25 ± 9.6. The FHC was located medial to the acetabular rim in 408 hips (88.3%), superimposed in 52 (11.2%) and lateral to the acetabular rim in 2 (0.4%).

Correlation analysis

While no correlation was found between the age of the subjects and the evaluated parameters, a significant correlation was found among the evaluated parameters (Table 1).

Correlations of the FCI A and B groups in the entire population

The values (mean ± SD) of the parameters evaluated at EE for the hips with adult grades of FCI A and B were as follows: AR, 4.42° ± 6.0° vs 7.62° ± 7.2°; AS, 0.45° ± 1.9° vs 1.55° ± 3.8°; LI, 0.32 ± 0.1 vs 0.36 ± 0.1; DARS, 3.30° ± 1.8° vs 3.77° ± 1.9°; and TS, 11.47 ± 8.3 vs 16.65 ± 10.9. In the FCI group, the FHC at EE was located medial to the acetabular rim in 278 hips (91.7%), superimposed in 24 (7.9%), and lateral to the acetabular rim in 1 (0.3%). In the FCI group, the FHC at EE was located medial to the acetabular rim in 130 hips (81.8%), superimposed in 28 (17.6%), and lateral to the acetabular rim in 1 (0.6%). The values of all the parameters tested at EE were significantly lower in the FCI A than in the FCI B group (p p = 0.01 for DARS). In addition, the FCI A group had significantly more medially located FHCs (p Fig 1. For better visualization, the values of the parameters of the FCI A and FCI B hips are summarized in Table 2.

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Fig 1. Values of the parameters at the time of early evaluation.

1: AR (°), 2: AS (°), 3: LI, 4: DARS (°), and 5: TS. The blue bars represent the entire population: the red bars, the FCI A group: and the green bars, the FCI B group. * Significant difference in the evaluated parameters between the FCI A and B groups.

https://doi.org/10.1371/journal.pone.0233257.g001

Differences between the breeds

The Labrador Retrievers and Golden Retrievers showed significant differences in all the parameters between the FCI grades. In particular, the FCI B group had significantly higher AS in both breeds (p = 0.03 and p = 0.04, respectively), LI (p = 0.01 and p = 0.01, respectively), and TS (p p = 0.03, respectively). Among the Labrador Retrievers, the FCI B group had significantly higher AR and DARS (both p Table 3.

The Border Collie group showed negative correlations between age and AR (r = −0.33, p = 0.03) and TS (r = −0.34, p = 0.027) in the FCI A group. By contrast, the Labrador Retrievers showed positive correlations between age and AR (r = 0.20, p = 0.02) and TS (r = 0.17, p = 0.04) in the FCI A group. Only the Golden Retrievers showed a positive correlation between age and LI (r = 0.44, p

The between-breed comparisons in the FCI A group showed that the AR and TS of the Labrador Retrievers were significantly higher than those of the Bernese Mountain Dogs (p p p p

Probability of prediction of FCI A and B hips

Fig 2 shows the predicted probabilities for FCI A or B hips according to the TS of the whole cohort and separately for the two breeds that showed significant differences in TS, namely the Labrador and Golden Retriever. For the entire cohort, TS had a high influence on the final FCI grade (p Table 4 provides the results of the logistic regression analysis in more detail.

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Fig 2. Probability curves of the entire population, Golden Retriever, and Labrador Retriever.

Probability graph for the entire population (1), Golden Retrievers (2), and Labrador Retrievers (3): The dark and light dotted lines represent the probabilities for the development of FCI A and B hips, respectively. The green square marks the zone in which the probability is between 45% and 55%. In this zone, the score range from 22 to 28 for the entire population, from 6 to 14 for the Golden Retrievers, and from 28 to 35 for the Labrador Retrievers.

https://doi.org/10.1371/journal.pone.0233257.g002

Fig 2 highlights the TS range for which prediction is difficult and wherein A and B overlap. This uncertain range is differs when considering the entire cohort (TS, 22–28), Labrador Retrievers (TS, 28–35), and Golden Retrievers (TS, 6–14).

Discussion

The objective of this study was to verify whether EE can reveal differences in the evaluated parameters in skeletally immature hips [41] that are classified as FCI A and B in adult dogs. The entire multi-breed cohort and Labrador Retriever breed group showed that hip joints classified as FCI B had significantly higher AS, AR, LI, DARS, and TS at EE. The Golden Retriever breed group showed significantly higher AS, LI, and TS at EE only for the FCI B hips. As only normal and near-normal hips were evaluated, only minimal differences were expected. Another key finding of our study was that for the entire cohort, the FHC was significantly more often located medial to the acetabular rim in the FCI A hips.

The study also evaluated the influences of age and breed on the different parameters, and showed that in the entire cohort, age had no influence. In the breed groups, some influences were observed for both FCI grades. In the Border Collie FCI A subgroup, the correlations of age to AR and TS were negative, possibly because the breed is not highly predisposed to CHD. Meanwhile, with increased age, the AR and TS of the subgroup seemed to be decreased, showing a lower score in the measurements performed to quantify the joint laxity. To the best of our knowledge, no study has been conducted on CHD predisposition in this particular breed. By contrast, the Labrador Retriever FCI A subgroup showed positive correlations between age, and AR and TS, possibly reflecting the predisposition of this breed to an increased hip laxity and, subsequently, to CHD. The Golden Retriever FCI B subgroup showed a positive correlation between age and LI. This is contrary to the prevailing logic that age and LI should be negatively correlated, as hip laxity decreases over time due to capsular tightening and fibrosis [4,42], but is in concordance with a recent study [43]. The short period between the EE and the final examination in this study did not provide enough time for the development of capsular tightening of fibrosis [44]. An alternative explanation would be that in juvenile patients with a transitional coxofemoral hip joint, synovitis (even at low severity) can lead to increased laxity [3,4]. These aspects should be considered in subsequent studies with high number of cases and precise analysis of the broad array of etiological factors (i.e., muscle mass, growth rate, and environmental factors). Similar to our findings that age has a different correlation to laxity, a recent study [43] showed significant variations in DI values in dogs between 4, 6, and 12 months of age. Taroni et al. found that this parameter increased between 4 and 6 months of age but decreased between 6 and 12 months of age.

The most noteworthy differences observed in the evaluated parameters in this study were between the Labrador Retriever and Golden Retriever breed groups. This could be an artifact of our study cohort’s overrepresentation of the former breed; however, the latter breed is similar in size to the other two breeds examined (Bernese Mountain Dog and Border Collie). Nonetheless, the differences observed between the measured parameters in all the breeds were statistically relevant for hips that were not significantly different from a pathological standpoint (i.e., normal and near-normal hips) and indicate the importance of differentiating between breeds. It is still intriguing that Labrador Retrievers showed distinctive differences, which may indicate that EE prediction is more readily adoptable to this breed in particular.

The features of FCI A and B hips are very similar, which makes the distinction between them difficult. Our results suggest that using a TS instead of the single parameters in the EE, seems to improve the possibility of differentiating between these two grades according to differences in the probability curves constructed for the entire cohort, Golden Retriever, and Labrador Retriever. This is in accordance with a previous study [19] that applied the parameters to a global predictive score. Collectively, these findings confirm that several parameters are needed to predict CHD development [15,18,19,31,38,43,45]. Similarly to the previous study [19], our stud demonstrated that the TS summarized all the measured values and, up to a certain score, showed a predictive ability. The TS range where the probability was almost equal for predicting FCI A and B hips represents its weakness. This range was different for the entire cohort, Labrador Retrievers, and Golden Retriever. For the entire cohort and Labrador Retriever group, the distinctive range is sufficiently large to predict an FCI A hip; for Golden Retrievers, the indistinctive range is large, leaving only a small range for accurate prediction of the development of FCI A hip. Thus, for the Golden Retrievers, either differentiating between FCI A and FCI B is not possible when the TS is low or only prediction of FCI B or worse is possible when the TS is >20; prediction of an FCI A hip is uncertain with a low TS. This result also agrees with the previous study wherein the probability curves were calculated for all FCI grades [19]. A recent study showed that measurements in the distraction view, performed in the EE, can predict, FCI A, B or C in adult dogs [31], but are not accurate predictors of FCI grade at 12 months of age. In this study, 96% of the hips wi De afleidingsindex van

Onze resultaten met hogere parameterwaarden voor FCI B-heupen komen overeen met eerder gepubliceerde resultaten [ 18 , 19 ]. Sommige waarden die we bij EE verkregen voor FCI A- en FCI B-heupen, zoals de gemiddelde AR van respectievelijk 4,42 ° ± 6,0 ° en 7,62 ° ± 7,2 °, waren over het algemeen lager dan de AR van 15 ° in de vorige onderzoek [ 19 ]. De vorige studie gebruikte een opmerkelijk kleinere groepsgrootte [4-11 honden] en sloot honden die negatief testten op het Ortolani-teken uit van de statistische analyse. De gemiddelde AS in ons onderzoek was analoog aan die beschreven in het vorige onderzoek [ 19 ], en de gemiddelde LI in ons onderzoek was vergelijkbaar met de gepubliceerde DI-waarden in andere onderzoeken [ 19 , 46 ]. Voor LI bevestigden onze bevindingen niet alleen de conclusie van Smith et al. dat honden met een DI van 0,3 al dan niet degeneratieve gewrichtsaandoeningen ontwikkelen [ 38 ] maar ben het ook eens met een recent onderzoek dat heeft vastgesteld dat een drempel van 0,58 voor DI de FCI A-, B- en C-heupen [ 31 ] nauwkeurig kan voorspellen. De LI-waarden in de huidige studie kunnen worden vergeleken met de DI-waarden in de vorige studies, aangezien een vergelijkbare interobserver-overeenkomst had kunnen worden aangetoond [ 33 ]. Een andere studie [ 47 ] met 313 honden vond een lage tot matige correlatie tussen de resultaten van het Ortolani-teken en de FCI-heupgraad. Het Ortolani-teken werd positief getest bij 31 (12,3%) van de 252 honden die werden geclassificeerd met een FCI A- of B-heup. In tegenstelling tot onze studie gebruikte de vorige studie alleen het Ortolani-teken als een kwalitatieve meting, zonder de resulterende laksheid in de AR te kwantificeren. De honden die op het Ortolani-teken werden getest, waren in het vorige onderzoek ≥12 maanden oud, terwijl de honden die in ons onderzoek aan metingen waren onderworpen, nog geen volwassen skelet hadden bereikt.

Ons onderzoek heeft beperkingen die onze bevindingen mogelijk hebben beïnvloed. Deze omvatten voornamelijk de niet-uniforme verdelingen van de FCI A- en B-heupen tussen de groepen, met een groter aantal FCI A-heupen, en de beoordeelde rassen (met name het aanzienlijk hoge aantal Labrador Retrievers) en hun FCI A- en B-heupen binnen elke groep. De duidelijke resultaten voor de voorspelling van definitieve FCI A- en B-cijfers en algemene verschillen in parameters tussen FCI A en FCI B in de Labrador Retriever-groep geven de noodzaak aan van onderzoeken met grote homogene groepen om de standaardparameterwaarden te bepalen. De lange tijdsspanne van de EE in deze studie, tussen de 3 en 7 maanden oud, zou een beperking kunnen zijn, hoewel deze de normale klinische routine weerspiegelt. Leeftijd had echter geen invloed op de parameters in ons onderzoek, met uitzondering van de Golden Retrievers met FCI B-heupen. Voor een nauwkeurige schatting van de invloed van leeftijd is verder onderzoek nodig bij een breder scala aan hondenrassen in verschillende levensfasen en groepen die voldoende groot zijn voor statistische analyse. Enkele andere beperkingen waren te wijten aan het retrospectieve karakter van het onderzoek, zoals het feit dat de metingen niet door één enkele onderzoeker zijn uitgevoerd. Desalniettemin hebben LI-metingen een goede herhaalbaarheid en reproduceerbaarheid aangetoond, met een lage intraobserver- en interobservervariabiliteit [ 48 , 49 ].

Onze resultaten geven aan dat rassen zelfs bij normale en bijna normale heupen significante verschillen vertoonden, die de aanleg van sommige rassen voor een hogere heuplaxiteit op jonge leeftijd kan weerspiegelen, wat kan leiden tot degeneratieve gewrichtsaandoeningen [ 2 , 50 ]. Hoewel eerdere studies rassen met een hoger risico op CHD vergeleken met rassen waarvan bekend is dat ze een lage incidentie van CHD hebben [ 39 , 51 ], er zijn meer onderzoeken nodig om duidelijke waarden voor de verschillende rassen vast te stellen.

Conclusies

Als de waarden van de parameters die in de EE worden gebruikt, worden omgezet in een TS, kunnen ze een voorspellende waarde bieden, maar wees voorzichtig, want de TS is sterk afhankelijk van het ras. Daarom kunnen er in het algemeen geen aanbevelingen worden gedaan voor rassen. Verdere studies met meer rassen en grotere steekproeven zijn nodig om een ​​algemene verklaring op te stellen over de relevantie van elke parameter voor individuele rassen. Op basis van de resultaten van ons onderzoek kunnen we alleen het gebruik van verschillende parameters aanbevelen om de heuplaxiteit bij opgroeiende honden te onderzoeken.

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