Computed tomography ndings in a cohort of 169 dogs with elbow dysplasia

Background: Canine elbow dysplasia (CED) is a complex developmental skeletal disorder associated with a number of pathological conditions within the cubital joint in dogs. Complex primary conditions associated with CED included medial coronoid disease without fragmented medial coronoid process, medial coronoid disease with fragmented medial coronoid process, osteochondrosis and/or osteochondrosis dissecans, ununited anconeal process, and joint incongruency and may be identied separately as a singular cause of elbow dysplasia, or occur as a combination of lesions presented simultaneously. The objective of this study was to assess the percentage prevalence of different components of CED in dogs suffering from this condition with the use of CT imaging. In addition, the correlations between various CED lesions and demographic features of the tested dogs were investigated. Results: 169 dogs of various breeds met the inclusion criteria. Statistically signicant differences were found between the age of affected dogs in individual weight groups. Moreover, the signicant correlation between weight and age in the cohort of large-size dogs with CED was noted. In 96 dogs OA of varying severity was found. 11.6% of dogs were diagnosed with unilateral CED and 88.4% suffered from bilateral CED. The majority of dogs diagnosed with CED were young with an average age of 2.26 ± 0.18 years old. Signicant differences in the occurrence of CED components in different-size groups were also noted. Males represented the majority in this study population. Conclusion: CT-imaging allowed for the assessment of the prevalence of CED components in affected dogs of different breeds. The use of CT imaging as a screening test in puppies of the breeds of which CED is the most prevalent facilitates the selection of dogs with joint incompatibility, which increases the risk of MDC, at time when no other changes are present. An early diagnosis of the mentioned pathology may allow for the introduction of less invasive therapeutic strategies, ensuring the improvement of joint biomechanics. The correlation between different components of CED and demographic features found in our study may provide valuable prognostic criteria and help in the future identication of various risk factors or therapeutic strategies.


Background
Canine elbow dysplasia (CED) is a prevalent health issue that affects many breeds, particularly medium to large sized dogs, however it is also reported in smaller chondrodystrophic breeds like the Dachshund and French bulldog [1,2,3]. Elbow dysplasia is relatively common in dogs and has a reported prevalence of 17% in UK Labradors [4,5], 70% in Bernese mountain dogs [6], 13% in Belgium Labradors and 26% in Belgium Newfoundlands [7]. Several research reports con rmed that certain breeds tend to be affected by a particular entity more frequently than others [2,7,8].
CED is a complex developmental skeletal disorder associated with a number of pathological conditions within the cubital joint in dogs [1,9,10]. Complex primary conditions associated with elbow dysplasia included medial coronoid disease without fragmented medial coronoid process (MCD), medial coronoid disease with fragmented medial coronoid process (FMCP), osteochondrosis (OC) and/or osteochondrosis dissecans (OCD), ununited anconeal process (UAP), and joint incongruency (INC) and may be identi ed separately as a singular cause of elbow dysplasia, or occur as a combination of lesions presented simultaneously [1,11].
Elbow dysplasia can cause severe lameness, and arthroscopic treatments do not palliate pain in all affected dogs [12,13]. Because CED is a heritable disease, it is very important to identify and remove the affected animals from breeding to decrease the prevalence of CED in dogs. Although some lesions, including UAP and OCD of the humerus, are quite often successfully identi ed on plain radiographs, appropriate diagnosis of the MCD or FMCP may be less straight-forward due to superimposition of medial epicondyle and muscle tissue [14]. Computed tomographic imaging is recognized as a high-sensitivity tool that allows for a detailed visualization of the skeletal components of the joints [11,15,16,17]. Moreover, computer tomography (CT) enables not only detection but also monitoring of progression in elbow dysplasia [16]. Recently, the use of CT has become increasingly widespread in veterinary medicine. Current data indicate that various components of CED (i.e. MDC) might be detected as early as 14 weeks of age. Early diagnosis is important from a therapeutic point of view, as lesions must be detected before severe osteoarthritis (OA) develops to achieve the most effective treatment outcomes [18]. However, the number of CTbased studies assessing prevalence of different CED lesions in dogs, including dogs of different breeds is limited [19,20]. Evaluation of potential correlations between certain components of CED and speci c demographic and/or phenotypic features may allow for more appropriate research in the future and ultimately lead to the identi cation of new risk factors and underlying molecular mechanisms [21].
The objective of this study was to assess the percentage prevalence of different components of CED in dogs suffering from this condition with the use of CT imaging. In addition, the correlations between various CED lesions and demographic features of the tested dogs were investigated.

Animals
The study was conducted on 169 dogs of different breeds admitted to the small animal veterinary clinic (Klinika Psa i Kota, Wrocław, Poland) from February 2012 to November 2018, for diagnostic CT imaging due to bilateral or unilateral elbow lameness. Only dogs diagnosed with CED were included in the study. Animals with non-CED associated elbow lameness, were excluded from the investigation. The exclusion criteria were non-CED associated elbow lameness (i.e. traumatic bone or soft tissue injury within this region, lameness due to neurological conditions). In addition, dogs with coexisting metabolic conditions that may have resulted in signi cant risks for anesthesia were also excluded from the study. Study design For each dog the following data were gathered: breed, age, sex and weight. Detailed characteristics of dogs included in the study are presented in Table 1. 169 dogs with CED were divided into three different size categories: medium (11-25 kg, n = 16), large (26-44 kg, n = 120) and extra-large (≥45 kg, n = 31). All dogs underwent physical and orthopedic examinations followed by a complete blood count and serum biochemistry tests. The assessment of mobility function and presence of lameness was performed by a veterinary surgeon. All study participants were able to walk without assistance.
Owners obtained a written description of the study and they provided written informed consent for the inclusion of their dogs in the study.

CT imaging and analysis
The prevalence of lesions such as: UAP, OCD, MCD, FMCP, radio-ulnar incongruence (INC R-U); humero-ulnar incongruence (INC H-U) and panosteitis (PANOS) was estimated on the basis of the results of CT imaging. MCD and FMCP lesions were analyzed separately. The degree of OA was also assessed based on International Elbow Work Group (IEWG) guidelines [22]. A total of 338 elbow joints was screened with CT-imaging.
CT images were obtained with a 2-slice helical scanner (Twin, Elscint, Israel) and 16-slice helical scanner (Somatom, Siemens. Germany) using 120 kVp or 110 kVp, 100 mA, pitch 0.8 and reconstructed slices were 0.6 mm with an overlapping slice index of 0.5 mm for reconstructing the imaging planes, after initial the scan. Dogs were sedated with intramuscular injection (i.m) of medetomidine in a dose of 5-20 µg (micrograms)/kg and butorphanol (0.1-0.4 mg/kg). Induction was obtained with propofol in a dose of 3.2 mg/kg of body weight administered intravenously followed by endotracheal tube placement. Iso urane and 100% oxygen were used for anesthesia maintenance. Dogs were placed in sternal recumbency with both thoracic limbs extended cranially and head was shifted out of the gantry to avoid potential artefacts. DICOM les of each scan were analyzed by an experienced veterinary radiologist using 3D MPR tool in OsiriX (64-bit software, Pixmeo, Geneva, Switzerland) to evaluate the scans in saggital and dorsal planes.
The level of OA in each elbow joint was scored according to IEWG [22] and the following scores were assigned: 0normal elbow joint (no evidence of incongruity, sclerosis or arthrosis); 1-mild arthrosis or suspect primary lesion (presence of osteophytes < 2 mm, sclerosis of the base of the coronoid processes -trabecular pattern still visible); 2-moderate arthrosis (presence of osteophytes 2-5 mm, obvious sclerosis (no trabecular pattern) of the base of the coronoid processes, step of 3-5 mm between radius and ulna (incongruity), indirect signs for other primary lesion (UAP, FMCP/coronoid disease, OCD); 3-severe arthrosis or evident primary lesion (presence of osteophytes > 5 mm, step of > 5 mm between radius and ulna (obvious incongruity), obvious presence of a primary lesion (UAP, FMCP, OCD) (8).  11.6% of dogs were diagnosed with unilateral CED and 88.4% suffered from bilateral CED. Two dogs (1.18%) were identi ed with bilateral panosteitis and four (2.37%) with unilateral panosteitis in addition to CED lesions.
The percentage distribution of CED lesions across the population of dogs included in the study is shown in Fig. 1. Signi cant differences in the occurrence of CED components in different-size groups were found (p < 0.0001).
Prevalence of CED components within breeds and in single-digit breed representants is presented in Tables 2 and 3, respectively.

Discussion
In the present study the CT imaging was used for assessing the prevalence of various CED components in dogs affected by CED. Moreover, the relationship between speci c demographic features and CED components in a cohort of 169 dogs was analyzed. Taking into account the hereditary occurrence of elbow dysplasia in dogs [23], it is very important to have diagnostic techniques allowing for a precise diagnosis of all CED cases, which will ensure a proper identi cation of animals with dysplasia and their elimination from breeding. Particularly, some earlier studies have demonstrated that CT is more sensitive in detection of MCD compared to radiographs [15,16,17]. It is widely accepted that CT is of a higher diagnostic quality for diagnosing elbow dysplasia, the IEWG currently does not recognize a standardized method of obtaining CT images of the elbow to be used in the screening process [1]. On the other hand it is known, that the joint congruency may be affected by positioning and slice thickness of the CT used. The researches within this area are needed to evaluate and elaborate the most accepted and accurate protocol for CED screening using CT. The prevalence of CED could be decreased with more widespread and accurate screening of the parents and/or more cautious selection of dogs for breeding. The early diagnosis will also contribute to better treatment outcomes [18].
Computed tomography imaging performed in a large cohort of CED -affected dogs allowed for assessment of prevalence of different CED components for each breed and across the whole population of dogs included in this study. In accordance with previous ndings, in the present study the elbow dysplasia was more common in males than in females. [20]. It is hypothesized that sex distribution is associated with dominant inheritance within male linage [24]. The demographic data demonstrate inclusion of dogs of typical breeds (mostly large breeds) affected by CED, with wide range in age and severity of pathology. In our study, similarly to data presented previously [25], Labrador Retrievers and GSD were within the most represented breeds in the veterinary clinic due to CED-associated lameness. In addition to CED, approximately 75% of dogs included in our study have been diagnosed with concurrent OA of different degrees. Previous ndings indicated that OA may develop as a primary lesion, although presence of degenerative changes is often directly associated with development and progression of CED [26].
Our study showed that 11.6% of dogs were diagnosed with unilateral CED and 88.4% suffered from bilateral CED. Humero-ulnar incongruence was identi ed as the most frequently identi ed CED-lesion across all breeds of dogs included in our study population. In our study, approximately 40% of dogs diagnosed with humero-ulnar incongruence were identi ed with MCD via CT imaging. Similar results were observed by Mostafa et al. (2019) in the study investigating populations of Labrador Retrievers and Golden Retrievers with the use of radiograph evaluation.
In the mentioned study, the co-presence of humero-ulnar incongruence with MCD was also observed [14].
Radio-ulnar incongruence was detected in 39.6% of dogs included in the present study, and approximately 50% of dogs with this lesion exhibited co-presence of fragmented medial coronoid process. Previous studies conducted by Eljack et al. (2013) showed, that up to 60% of dogs diagnosed with radio ulnar incongruence were simultaneously affected by the medial coronoid disease, which complies with our ndings [27]. Interestingly, 100% of the Chow Chow's recruited into our study (n = 6) were simultaneously identi ed with humero-ulnar incongruence and fragmented medial coronoid process. This may be associated with generally higher heritability values for this breed as has been shown previously [1]. Osteochondrosis dissecans (OCD) was detected in 11.24% of dogs and was always accompanied by other CED lesions. United anconeal process (UAP) was the least frequently identi ed lesion in our study population and accounted for approximately 9.46%. Similar prevalence for both OCD and UAP was reported in previous reports [8]. Concurrent occurrence of FCMP and UAP was previously reported to be rather sporadic ndings [28,29,30]. In the present study similar results were found. The simultaneous presence of FCMP and UAP was observed only in 3 dogs (GSD, Bernese Mountain Dog, Cane corso). Interestingly, several breeds were presented with CED -associated lameness in older age than others in the present study. Speci cally, Boxers, Dog de Bordeaux, American Staffordshire Terriers and crossbreed dogs have been identi ed as a late-life CED onset group.
The age-associated peak for CED has been reported previously [31]; however, the data describing speci c breeds are limited. Due to a small number of dogs from breeds which represented late-onset of CED in our study (5 Boxers, 5 Dog de Bordoux, 3 American Staffordshire Terriers and 2 crossbreed dogs) more research is needed to con rm these ndings.
To summarize, the various CED lesions were found across the population of dogs included in the present study. INC H-U, FMCP and MCD were found to be the most common (in 129, 92 and 89 dogs, respectively). OCD and UAP were the least frequently identi ed pathologies (in 19 and 16 dogs, respectively). The correlation between different components of CED and demographic features found in our study may provide valuable prognostic criteria and help in the future identi cation of various risk factors and relevant therapeutic strategies. The use of CT imaging as a screening test in puppies of the breeds of which CED is the most prevalent (Labrador, GSD, Bernese Mountain Dog) facilitates the selection of dogs with joint incompatibility, which increases the risk of MDC, at time when no other changes are present. An early diagnosis of the mentioned pathology may allow for the introduction of less invasive therapeutic strategies, ensuring the improvement of joint biomechanics [32]. According to the Act on the Protection of Animals Used for Scienti c or Educational Purposes in Poland adopted on 15th January 2015 and according to earlier regulations the study described in this manuscript did not require permission of the Local Ethical Commission for Investigations on Animals. Written informed consent to participate was obtained from the all participants.

Consent for publication
Written informed consent for publication of their clinical details and images was obtained from all the owners of the patients.

Availability of data and material
The data used to support the ndings of this study are available from the corresponding author upon reasonable request.

Competing interests
The authors declare that there is no con ict of interest regarding the publication of this paper.