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    Figure 1

    A representative example of axial CT images (bone reconstruction) delineating regions (arrowheads) around the medial coronoid process (A) from apex to base and the proximal radial cortex (B) at the level of the nutrient foramen (arrow) used to quantify attenuation.

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    Figure 2

    Flow diagram outlining case recruitment for groups 1 and 2, and the final classification of included elbow joints by arthroscopic disease classification (Modified Outerbridge score [MOS]).

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    Figure 3

    Box-and-whisker plot showing attenuation of the medial coronoid process (MCP) (measured in Hounsfield units) within and between categories of arthroscopic disease severity. MOS = Modified Outerbridge score.

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    Figure 4

    Box-and-whisker plot showing attenuation of the medial coronoid process (MCP) normalized to the attenuation of the proximal radial cortex (PRC) (measured in Hounsfield units/Hounsfield units) within and between categories of arthroscopic disease severity. MOS = Modified Outerbridge score.

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CT attenuation of the medial coronoid process is reduced in dogs with medial coronoid disease but independent of arthroscopic disease severity

William J. HumphreysSmall Animal Teaching Hospital, School of Veterinary Science, Institute of Veterinary and Ecological Sciences, University of Liverpool, Leahurst Campus, Neston, UK

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Katie WilderAvon Lodge Veterinary Group, Salisbury, UK

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Rob PettittSmall Animal Teaching Hospital, School of Veterinary Science, Institute of Veterinary and Ecological Sciences, University of Liverpool, Leahurst Campus, Neston, UK

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Eithne J. ComerfordSmall Animal Teaching Hospital, School of Veterinary Science, Institute of Veterinary and Ecological Sciences, University of Liverpool, Leahurst Campus, Neston, UK
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Thomas W. MaddoxSmall Animal Teaching Hospital, School of Veterinary Science, Institute of Veterinary and Ecological Sciences, University of Liverpool, Leahurst Campus, Neston, UK
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Abstract

OBJECTIVE

To compare the attenuation of the medial coronoid process (MCP) in dogs with and without arthroscopically confirmed evidence of medial coronoid disease (MCD).

ANIMALS

The database at our institution was searched for cases with thoracic limb lameness, diagnosed with MCD by arthroscopic examination that had CT as part of their investigation and compared with a control group of elbow joints from cadavers euthanized for reasons unrelated to MCD. A total of 84 elbow joints were included that met these criteria.

PROCEDURES

Following CT, a standardized measurement of the MCP was obtained from apex to base and the mean attenuation, SD, and total area were recorded. A comparative measurement was obtained from the proximal radial cortex at the level of the nutrient foramen. Elbow joint arthroscopy was carried out using standard portals, and the modified Outerbridge score was (MOS) used to score elbow joint cartilage. Descriptive and inferential statistics were carried out using MLwiN and R.

RESULTS

Attenuation of the MCP was reduced in dogs with MCD compared with those with no MCD (P < .002). No significant differences were observed in the attenuation between categories of severity (MOS). There was good inter- and intraobserver agreement between measurements (intraclass correlation coefficient = 0.89 and 0.95, respectively).

CLINICAL RELEVANCE

MCP attenuation is reduced in dogs with MCD compared with dogs with no evidence of MCD. This finding may be a useful tool for early detection of MCD, but there is no relationship with arthroscopic lesion severity.

Abstract

OBJECTIVE

To compare the attenuation of the medial coronoid process (MCP) in dogs with and without arthroscopically confirmed evidence of medial coronoid disease (MCD).

ANIMALS

The database at our institution was searched for cases with thoracic limb lameness, diagnosed with MCD by arthroscopic examination that had CT as part of their investigation and compared with a control group of elbow joints from cadavers euthanized for reasons unrelated to MCD. A total of 84 elbow joints were included that met these criteria.

PROCEDURES

Following CT, a standardized measurement of the MCP was obtained from apex to base and the mean attenuation, SD, and total area were recorded. A comparative measurement was obtained from the proximal radial cortex at the level of the nutrient foramen. Elbow joint arthroscopy was carried out using standard portals, and the modified Outerbridge score was (MOS) used to score elbow joint cartilage. Descriptive and inferential statistics were carried out using MLwiN and R.

RESULTS

Attenuation of the MCP was reduced in dogs with MCD compared with those with no MCD (P < .002). No significant differences were observed in the attenuation between categories of severity (MOS). There was good inter- and intraobserver agreement between measurements (intraclass correlation coefficient = 0.89 and 0.95, respectively).

CLINICAL RELEVANCE

MCP attenuation is reduced in dogs with MCD compared with dogs with no evidence of MCD. This finding may be a useful tool for early detection of MCD, but there is no relationship with arthroscopic lesion severity.

Canine elbow dysplasia (CED) is an umbrella term first defined by the International Elbow Working Group.1 It encompasses multiple developmental anomalies of the canine cubital joint, including ununited anconeal process, humeral osteochondrosis, articular cartilage injury, elbow incongruity, and fragmentation of the medial coronoid process (FMCP).26 CED results in chronic thoracic limb lameness in young, large breed dogs secondary to irreversible arthritis and is a significant cause of morbidity in this population.3,4,79 It is also reported in some chondrodystrophic small-breed dogs.4,10

FMCP is the most common heritable form of CED.11,12 Recently, this term has been superseded by medial coronoid disease (MCD)—a broader term that incorporates the wide spectrum of cartilage pathology associated with the medial coronoid process (MCP), of which fragmentation is the end stage.13 The etiopathogenesis of MCD has been widely debated, with incongruity of the elbow joint postulated to be the most likely cause. Humeroulnar incongruity and trochlear notch deformity,14 radioulnar incongruity,4,15 and primary rotational incongruity16,17 have all been suggested as possible inciting causes, with or without concurrent defects in endochondral ossification.18 Regardless of the aberrant anatomic conformation, a supraphysiologic load is placed on the MCP, causing subchondral microfractures and ultimately grossly evident fissures, and these features have been observed histologically19 and by using micro-CT.20

The diagnosis of MCD remains challenging, with direct examination of the medial compartment via arthroscopy (alone or in combination with additional imaging) remaining the gold standard.11 Radiography has been the standard modality used for diagnosis, grading, and screening for CED and MCD, but interpretation is confounded by the superimposition of the complex three-dimensional anatomy of the elbow joint.2 It is rare to see a discrete osteochondral fragment with MCD; therefore, radiographic diagnosis of MCD, and FMCP, is based on the detection of secondary signs. These include proximal anconeal osteophytosis, proximal radial osteophytosis, subchondral sclerosis of the semilunar notch, and alterations in the radiographic silhouette and lucency of the MCP alongside exclusion of other primary causes such as ununited anconeal process and osteochondrosis.2

Consequently, other advanced imaging modalities have been used in the detection of MCD, both qualitatively and quantitatively. CT has been widely investigated, alleviating issues with superimposition and permitting multiplanar reconstruction of acquired images.2,21 In a recent study,22 CT was reported to have a sensitivity of 100% and specificity of 93% compared with arthroscopy for the assessment of MCD, and it also permits quantification of incongruency.2326 In parallel, MRI permits imaging in multiple planes with exquisite soft tissue detail, with superior contrast resolution available from combinations of multiple sequences.26 MRI is more sensitive than radiography for detection of an abnormal MCP,27 and a recent report highlighted a statistically significant correlation between articular cartilage lesions observed with MRI and modified Outerbridge score (MOS) at arthroscopic examination.28 However, its clinical applications remain limited by its cost, prolonged anesthetic time, and limited availability.

Quantitative assessment of the density of the MCP has been investigated in vivo, with dual-energy x-ray absorptiometry and CT using both osteoabsorptiometry (CTOAM) and Hounsfield units to infer bone mineral density (BMD).5,6,8,29 The Hounsfield unit is a standardized linear attenuation coefficient scale defining air as –1,000 and purified water as 0, with greater values correlating to increased BMD and vice versa.29 A recent topographic study6 quantifying the attenuation of the MCP, suggested a caudolateral load transfer in elbow joints affected with MCD, and a lower overall BMD. The potential utility of CT to provide further insights into the underlying pathophysiology of CED, and as a noninvasive semiquantitative screening tool for subclinical disease, should not be underestimated.

The aim of this study was to assess the attenuation of the MCP in dogs with and without MCD. The null hypothesis is that there would be no overall difference between the attenuation of the radial cortex and the MCP in dogs with and without MCD.

Material and Methods

Case recruitment

For assessment of the attenuation of the MCP in a population of dogs with confirmed MCD, the clinical records database at our institution was searched for cases that presented with thoracic limb lameness subsequently diagnosed with MCD by arthroscopic examination. Cases were included if they had a CT examination of one or both elbow joints and subsequent arthroscopic confirmation of MCD in the same elbow joint or joints. The full signalment of each patient was recorded.

In the control population, both elbow joints were scanned from a population of canine cadavers euthanized for reasons unrelated to thoracic limb disease. Elbow joints were scanned within 24 to 48 hours of euthanasia and stored at 4°C until required. Arthroscopic examination was performed immediately following CT scanning.

Ethical approval was received from the University of Liverpool Veterinary Ethics Committee under reference RETH000553.

Imaging and arthroscopic examination

Computed tomography

CT was performed routinely for both cases and control animals using the standard protocol at our institution. An 80-slice CT scanner (Toshiba Aquilon, Toshiba Medical Systems) was used to scan each elbow joint, with the patient positioned in sternal recumbency and the elbow joint in extension. The scan field of view was adjusted to extend from the proximal third of the radius to the distal third of the humerus of the elbow joint of interest. Typical acquisition parameters are included for reference—helical scan mode: pitch, 0.625; 50 to 70 mA; 100 to 120 kV; slice thickness, 0.5 to 1.0 mm; reconstruction kernel: sharp bone and soft tissue).

CT scan analysis

All images were reviewed retrospectively by a general practice veterinarian (observer 1) and an European College of Veterinary Diagnostic Imaging (ECVDI) resident in diagnostic imaging (observer 2) under similar guidance from a board-certified radiologist. Multiplanar reformatting was performed using proprietary image viewing software (Osirix 11.0, Pixmeo) for image analysis using the bone reconstruction and routine window width and length.30 Reviewers were blinded to the arthroscopic findings at the time of review. The attenuation (measured in Hounsfield units) of the caudoproximal radial cortex was measured using the polygon tool at the level at which the nutrient foramen perforates the ulnar cortex (Figure 1). The attenuation of the MCP was also measured using the polygon tool to outline a line parallel to but not including the medullary cavity of the ulna and around the MCP from apex to base on a single slice (Figure 1). Where gross fragmentation of the MCP was evident, any fragments were not included within the measurement area. The total area, mean attenuation, and SD were recorded at each site. One measurement at each site was recorded by observer 1, and 2 separate, and identical, measurements were recorded by observer 2. The arithmetic mean was calculated for the measurements across all observers and this value used for data analyses.

Figure 1
Figure 1

A representative example of axial CT images (bone reconstruction) delineating regions (arrowheads) around the medial coronoid process (A) from apex to base and the proximal radial cortex (B) at the level of the nutrient foramen (arrow) used to quantify attenuation.

Citation: American Journal of Veterinary Research 83, 9; 10.2460/ajvr.21.10.0171

Arthroscopic examination

A standard arthroscopic examination of each elbow joint was performed in cases and control animals to examine the medial and lateral compartments of the elbow joint using medial portals as described by Beale et al.31

Arthroscopic examination was carried out by a board-certified surgeon (European College of Veterinary Surgeons [ECVS] or Royal College of Veterinary Surgeons [RCVS]) or a resident under the supervision of a board-certified surgeon to provide direct observation of the MCP and confirmation of disease status. A modified Outerbridge cartilage grading system (MOS) (Table 1) was used to classify the pathology of the articular cartilage in the medial compartment of the elbow joint. The findings were recorded in a surgical report by the attending clinician immediately after examination.

Table 1

Table outlining the Modified Outerbridge score used to classify medial coronoid lesions arthroscopically

Modified Outerbridge score (MOS) Description of gross cartilage quality
0 Normal
1 Chondromalacia (assessed by use of an arthroscopic probe)
2 Partial thickness fibrillation
3 Deep fibrillation
4 Full-thickness cartilage loss (exposure of the subchondral bone)
5 Subchondral bone eburnation

Where pathological arthroscopic lesions were identified in presumptively normal cadaveric animals, these animals were regrouped and included in the dogs with confirmed MCD for statistical analysis (Figure 2).

Figure 2
Figure 2

Flow diagram outlining case recruitment for groups 1 and 2, and the final classification of included elbow joints by arthroscopic disease classification (Modified Outerbridge score [MOS]).

Citation: American Journal of Veterinary Research 83, 9; 10.2460/ajvr.21.10.0171

Statistical analysis

Statistical analysis was carried out using R (version 4.0.2, R Foundation for Statistical Computing) and MLwiN (version 3.02, Centre for Multilevel Modelling, University of Bristol).

Each elbow joint was treated as an individual case for statistical analysis and was classified into a group based on the MCD status as determined by the MOS, recorded immediately after arthroscopic examination. Elbow joints were initially categorized as normal (MOS = 0) or abnormal (MOS > 0). The abnormal group was then subclassified by MOS grade for further statistical analysis. As only a single case was assessed with an MOS = 4, this case was included with cases graded with an MOS of 3 to create a category of MOS of 3 or more for final analysis (Figure 2).

Primary outcome variables for data analysis between groups were mean attenuation (measured in Hounsfield units) and SD (measured in Hounsfield units) of the MCP and proximal radial cortex (PRC), and an arbitrary unitless value calculated to normalize the attenuation of the MCP to that of the PRC, calculated as MCP/PRC (measured in Hounsfield units/Hounsfield units).

Descriptive analysis was performed for all variables. The data were assessed for normality using visual histogram assessment, Q-Q plot analysis, and the Shapiro-Wilk test for normality. Based on the normality assessment, parametric testing was deemed appropriate. A paired t test was used to assess for significant differences between the attenuation of the PRC and MCP across all grading categories.

Interobserver variability between observer 1 and observer 2. and intraobserver variability for observer 2 was assessed by calculation of the intraclass correlation coefficient ([ICC] including 95% CIs) using a 2-way random effects model, as described by Koo and Li.32

Given the clustering of the data attributed to treating each elbow joint as a single case, multilevel linear regression analysis was deemed appropriate for assessing the relationships between the primary outcome variables, arthroscopic grade (MOS), and, ultimately, MCD status. Within-dog clustering of elbow joints was accounted for as a random intercept term in these 2-level models. P < .05 was considered significant in all analyses.

Results

Group 1: cases with arthroscopic evidence of MCD (MOS > 0)

A total of 42 dogs were identified from our institution with CT examination of one or both elbow joints, followed by contemporaneous arthroscopic examination. Dogs were between 6 months and 8 years 11 months. From these dogs, 64 elbow joints were assessed (22 cases with bilateral MCD and 20 cases with unilateral MCD). This group consisted of dogs weighing between 11.4 and 52 kg (mean, 31.05 kg). The data were normally distributed. Elbow joints examined in group 1 were from the following breeds: Labrador Retriever (n = 31), German Shepherd Dog (n = 6), Rottweiler (n = 6), cross-breed (n = 4), Boxer (n = 4), Bulldog (n = 3), English Springer Spaniel (n = 3), Cavalier King Charles Spaniel (n = 2), Bull Mastiff (n = 2), Cocker Spaniel (n = 2), and Labradoodle (n = 1).

After arthroscopic examination of the cadaveric control group, an additional 6 elbow joints from 5 dogs had evidence of MCD (1 case with bilateral MCD and 4 cases with unilateral MCD) and were moved to group 1, resulting in a total of 70 elbow joints examined in group 1. Prior medical history of these patients was unknown, but all were Staffordshire Bull Terriers (n = 6), skeletally mature and weighed between 18 and 30 kg.

Of 70 elbow joints, 37 had a MOS = 1, 22 had a MOS = 2, 10 had a MOS = 3, and 1 had a MOS = 4. No animals were examined with a MOS > 4. Because only a single case was examined with a MOS of 4, this case was pooled with those with a MOS ≥ 3 for final statistical analysis (Figure 2).

Group 2: cases with no evidence of MCD (MOS = 0)

The remaining (control) group of cadaveric animals consisted of 9 animals, with an assessment of 14 elbow joints. Prior medical history of these patients was unknown and dogs weighed between 18 and 30 kg (mean, 20.4 kg). All of these patients were skeletally mature. Elbow joints examined in group 2 were from the following breeds: Staffordshire Bull Terrier or Staffordshire Bull Terrier Crosses (n = 14). All 14 elbow joints in this group had a MOS = 0 (Figure 2).

Relationship between the attenuation of the MCP and PRC in dogs with and without arthroscopic evidence of MCD

The mean attenuation of the MCP and PRC across all arthroscopic grading categories were 1,361.94 HU and 1,581.73 HU, respectively. The data were normally distributed and the paired t test suggested that the overall attenuation of the PRC across all grading categories was significantly greater than the overall attenuation of the MCP (P < .001).

Relationship between the attenuation of the MCP in dogs with and without MCD

The distribution of the mean attenuation of the MCP in dogs with and without arthroscopic cartilage lesions is outlined in Table 2 and summarized in Figure 3. The data were normally distributed.

Table 2

Mean attenuation of the medial coronoid process (MCP) and mean attenuation of the MCP normalized to the proximal radial cortex across the arthroscopic grading category.

MOS Mean attenuation of the MCP (HU) Mean attenuation of the MCP normalized to the PRC (HU/HU)
0 (n = 14) 1,606.56(Ref) 0.86
1 (n = 37) 1,302.16* 0.89
2 (n = 22) 1,350.31* 0.83
≥ 3 (n = 11) 1,274.97* 0.86

HU = Hounsfield unit; MOS = Modified Outerbridge score; PRC = Proximal radial cortex.

*P < .002, significance from reference (MOS = 0).

Figure 3
Figure 3

Box-and-whisker plot showing attenuation of the medial coronoid process (MCP) (measured in Hounsfield units) within and between categories of arthroscopic disease severity. MOS = Modified Outerbridge score.

Citation: American Journal of Veterinary Research 83, 9; 10.2460/ajvr.21.10.0171

Multilevel linear regression analysis confirmed a significant relationship (P < .002) between the attenuation of the MCP in dogs with and without arthroscopic cartilage lesions. A significantly greater attenuation of the MCP in dogs scoring 0 at arthroscopy was noted compared with dogs that had MOS = 1, 2, or 3 (P < .002). However, no significant differences in attenuation were noted between the different severity categories of arthroscopically diseased elbow joints.

Relationship of the MCP normalized to PRC in dogs with and without MCD

The distribution of the mean attenuation of the MCP normalized to the PRC (MCP/PRC, measured in Hounsfield units) in dogs with and without arthroscopic cartilage lesions is outlined in Table 2 and summarized in Figure 4. The data were normally distributed.

Figure 4
Figure 4

Box-and-whisker plot showing attenuation of the medial coronoid process (MCP) normalized to the attenuation of the proximal radial cortex (PRC) (measured in Hounsfield units/Hounsfield units) within and between categories of arthroscopic disease severity. MOS = Modified Outerbridge score.

Citation: American Journal of Veterinary Research 83, 9; 10.2460/ajvr.21.10.0171

Multilevel linear regression analysis confirmed no statistically significant relationships between the mean attenuation of the MCP and arthroscopic categories when normalized to the mean attenuation of the PRC (P = .68).

Inter- and intraobserver variability

There was good interobserver reliability (ICC, 0.89; 95% CI, 0.66 to 0.95; P < .05) between the measurements of the attenuation obtained by observer 1 and observer 2. There was excellent intraobserver reliability (ICC, 0.95; 95% CI, 0.87 to 0.97; P < .001) between measurements taken by observer 2.

Discussion

The results of this study led us to reject our null hypothesis, concluding there was a significantly lower attenuation in the MCP and PRC in dogs with MCD compared with dogs without evidence of MCD upon arthroscopic examination of the elbow joint.

Bone is a dynamic tissue, responding to mechanical load via Wolff’s law.33 Accordingly, under normal physiologic conditions, reduction in BMD and therefore attenuation may reflect altered load within the osseous structures of the elbow joint. Phillips et al6 postulate a caudolateral load transfer within affected thoracic limbs as the physiologic mechanism underlying the reduction in overall attenuation of the MCP in dogs with MCD, a theory supported by the results of our study and the findings of the recent work by Wennemuth et al.34 We additionally found a parallel reduction in attenuation within the PRC, a finding supported by that of Villamonte-Chevalier et al28 in their population of Golden and Labrador Retrievers. This finding might further support the theory proposed by Phillips et al,6 given the roughly equal load sharing of the radius and ulna reported with in vitro force plate analysis in the canine elbow joint by Mason et al.35 A caudolateral load shift through the ulna could reasonably be expected also to unload the radius to a degree significant enough to result in reduced BMD. Alternatively, the hypoattenuation observed in our study might reflect an overall reduction in load on a thoracic limb unilaterally with contralateral weight shift, as might be expected with a degree of disuse osteopenia.36 However, this would require measurements of attenuation from additional distant locations not taken in our study and/or measurements from a population of dogs with true unilateral disease verified with force plate data.

Despite there being a significantly lower attenuation of the MCP and PRC in cases from our study with arthroscopic evidence of MCD, no significant relationship was shown for increasing severity categories of cartilage damage (MOS). This finding supports the results of a previous study in which imaging and arthroscopic evidence of disease were not correlative with clinical presentation.37 Our results suggest that reduced or altered load within a diseased elbow joint occurs consistently and repeatedly, but independent of actual arthroscopic disease severity. A clinical presentation score was not used in our study, and therefore association between clinical presentation and attenuation of the MCP could not be assessed. The reduction in attenuation independent of arthroscopic severity might support the adjunctive use of CT attenuation for early detection of reduced load bearing secondary to MCD, and the good inter- and intraobserver variability reported earlier demonstrates consistency in the technique described. However, it is clear from the literature that numerous factors, including age, breed, and disease course, affect the attenuation of the MCP; therefore, continued research is warranted in this area.6,38

There were several limitations to our study. A number of studies6,8,28,39 have reported variation in the bone density of the microstructure of the MCP in sagittal planes or zones. Although standardized, our measurement of the MCP consisted of a polygon drawn around the entire MCP from the apex to the base on a single slice, providing a general overview of the attenuation but potentially limiting insight into the variation in attenuation between zones of the MCP itself. Villamonte-Chevalier et al28 reported that the most consistent results were found when using the MCP base to make an assessment of the attenuation of the MCP, and further work should continue to optimize consistent and repeatable measurement locations for the MCP. This is of particular relevance given the presence of fissures (without overt fragmentation) through the MCP, which could conceivably reduce the attenuation when included within a region of measurement. It is also possible that variation in attenuation might occur between the MCP on adjacent slices and that assessment on a single slice might not have provided a representative measurement of the overall attenuation of the MCP. Last, CT has been shown to provide variable consistency in measurement of the attenuation of trabecular bone (up to 5% to 8%), and reduction of this value to ∼3% can be achieved with CTOAM and the use of a dipotassium phosphate standardization device.40 Although we believe this is unlikely to have affected the results of this study significantly, it is potential consideration for future work in this area.

There were further limitations inherent within the study population. First, the comparison of performing CT scans on cadavers with elbow joints scanned in vivo during clinical investigation may draw criticism. However, scanning frozen limbs postmortem has been shown to have no effect on the overall attenuation of trabecular bone identified by CT.40 We believe the benefit of contemporaneous arthroscopic examination for confirmation of disease status in normal animals (group 2) outweighs any negative impact of postmortem examination allowing accurate comparison of attenuation without subjecting a population of normal dogs to unjustified (in vivo) arthroscopic examination.40 Although the reliability of the MOS has been challenged in human arthroscopy, the intra- and interobserver reliability is reportedly high in canine patients, particularly in observers with extensive experience.41 Second, the overrepresentation of the Labrador Retriever breed in group 1 is a potential confounding factor. Phillips et al6 reported a significant difference in the attenuation of the MCP between a population of Greyhounds and Labrador Retrievers, suggesting significant interbreed variation in attenuation of the MCP. Ideally, breed matched case–controls would negate this bias, but this consideration was not practical for this study. Last, the lack of age data for group 2 is a potential limitation on conclusions from this study population. Dickomeit et al38 reported an age-dependent increase in subchondral bone density via CTOAM. It is possible that some degree of the parallel increase in attenuation of the MCP and PRC is a result of normal aging change, should a number of the cases in group 2 be significantly older than those in group 1. However, we believe that group 1 was sufficiently heterogeneous with regard to age to negate this hypothesis.

To conclude, we have reported a significantly lower attenuation in the MCP and PRC in dogs with evidence of MCD at elbow arthroscopy. CED is a complex multifactorial disease and it is clear that the attenuation pattern and BMD change dynamically throughout the disease course as a result of altered microstress/strain placed on the elbow joint. CT provides a noninvasive method to assess the attenuation of the bony structures of the elbow joint throughout the disease course. However, further research into the temporal changes in attenuation in individual cases followed longitudinally and among breeds is warranted before routine clinical implementation of this technique.

Acknowledgments

No third-party funding or support was received in connection with this study or the writing or publication of this manuscript.

The authors declare that there were no conflicts of interest.

We acknowledge Ben Jones and Lee Moore at the Veterinary Teaching Suite for their assistance with the cadaveric samples.

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Contributor Notes

Corresponding author: Dr. Maddox (thomas.maddox@liverpool.ac.uk)