MRI FEATURES OF CERVICAL ARTICULAR PROCESS DEGENERATIVE JOINT DISEASE IN GREAT DANE DOGS WITH CERVICAL SPONDYLOMYELOPATHY

Authors

  • Rodrigo Gutierrez-Quintana,

  • Jacques Penderis

    Corresponding author
    • From the School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow,, UK
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Address correspondence and reprint requests to Jacques Penderis at the above address. E-mail address: Jacques.Penderis@glasgow.ac.uk

Abstract

Cervical spondylomyelopathy or Wobbler syndrome commonly affects the cervical vertebral column of Great Dane dogs. Degenerative changes affecting the articular process joints are a frequent finding in these patients; however, the correlation between these changes and other features of cervical spondylomyelopathy are uncertain. We described and graded the degenerative changes evident in the cervical articular process joints from 13 Great Danes dogs with cervical spondylomyelopathy using MRimaging, and evaluated the relationship between individual features of cervical articular process joint degeneration and the presence of spinal cord compression, vertebral foraminal stenosis, intramedullary spinal cord changes, and intervertebral disc degenerative changes. Degenerative changes affecting the articular process joints were common, with only 13 of 94 (14%) having no degenerative changes. The most severe changes were evident between C4–C5 and C7–T1 intervertebral spaces. Reduction or loss of the hyperintense synovial fluid signal on T2-weighted MR images was the most frequent feature associated with articular process joint degenerative changes. Degenerative changes of the articular process joints affecting the synovial fluid or articular surface, or causing lateral hypertrophic tissue, were positively correlated with lateral spinal cord compression and vertebral foraminal stenosis. Dorsal hypertrophic tissue was positively correlated with dorsal spinal cord compression. Disc-associated spinal cord compression was recognized less frequently.

Introduction

ervical spondylomyelopathy or Wobbler syndrome is common in Great Dane dogs and other large and giant breed dogs. The etiology of cervical spondylomyelopathy is unclear, but chronic spinal cord compression is the main factor leading to the clinical signs that range from cervical pain to nonambulatory tetraparesis.[1-3] Two main forms of spinal cord compression occurring for cervical spondylomyelopathy have been described. The first is disc-associated and occurs secondary to Hansen type II intervertebral disc degeneration. This is identified typically in middle-aged, large-breed dogs, with the Dobermann Pinscher being a typical breed.[1, 4, 5] The second form is osseous-associated and usually occurs secondary to proliferation of the vertebral arch, pedicles, or articular processes and is typically seen in young giant breed dogs, with Great Dane dogs affected frequently.[1, 2, 4-6]

Magnetic resonance (MR) imaging is the diagnostic imaging modality of choice for dogs with suspected cervical spondylomyelopathy.[5-7] The pathologic,[2, 8-10] radiographic,[2, 8, 9] myelographic,[7, 9] and MR imaging[4-7, 10] changes in dogs with osseous-associated cervical spinal compression have been described. Osteoarthrosis of the articular process joints is common in these patients. The significance of the degenerative changes in the articular process joints with regard to the development of spinal cord compression, foraminal stenosis, and intervertebral disc degeneration are unclear. In comparison with standard radiographs, MR imaging allows improved visualization and assessment of the articular process joints due to its capability to image the joint in the transverse plane, and MR imaging may therefore be used to evaluate and grade changes within the articular process joints.

In this study, our objectives were (1) to describe the degenerative changes evident on MR imaging of the articular process joints in a cohort of Great Dane dogs with a clinical diagnosis of cervical spondylomyelopathy and (2) to determine the frequency at which spinal cord compression, intramedullary spinal cord changes, intervertebral foraminal stenosis, and degenerative intervertebral disc changes occurred in association with degenerative changes of the cervical articular process joints.

Materials and Methods

Medical records from January 2007 to April 2011 were reviewed to identify Great Dane dogs with clinical signs suggestive of cervical spondylomyelopathy and which underwent MR imaging of the cervical spine. Thirteen dogs were identified. The mean age was 3.7 years with a median of 3.9 years (range: 9 months–8 years). There were six males (one neutered) and seven females (five neutered). All dogs had neurologic signs suggestive of cervical spondylomyelopathy that included 10 dogs with ambulatory tetraparesis and ataxia, two dogs with nonambulatory tetraparesis, and one dog with cervical pain. The mean duration of neurological signs prior to presentation was 69.6 days with a median of 30 days (range: 2–365 days). In all dogs, a diagnosis of cervical spondylomyelopathy was made on the basis of the clinical presentation and the findings of the MR imaging study.

MR imaging of the cervical spine was performed using a 1.5 Tesla system1. Cervical articular process joints were included in the analysis if T2-weighted (2160-5890/86-130; range TR/TE) MR images were acquired in both sagittal and transverse planes. Dorsal T2-weighted and sagittal or transverse T1-weighted (360-870/10-15; range TR/TE) pre- and postintravenous gadolinium injection (0.1 mmol/kg of gadopentetate dimeglubine)2 MR images were available in some dogs. All dogs were in dorsal recumbency with the thoracic limbs extended caudally. In all MR imaging studies, the transverse plane images were orientated perpendicular to the vertebral canal. The field of view ranged from 36 cm × 36 cm to 51.2 cm × 51.2 cm (sagittal plane) and 13 cm × 13 cm to 51.2 × 51.2 cm (transverse plane). The slice thickness varied from 3.5 to 4 mm (transverse plane) and 3 to 4 mm (sagittal plane) with an interslice interval of 0.3–0.5 mm. The number of transverse plane images per intervertebral disc region ranged from 5 to 8.

MR images were evaluated by both authors using an open-source PACS Workstation DICOM viewer3 and the final assessment was a consensus opinion. All available transverse plane images through an individual intervertebral disc region were evaluated. Changes within the articular process joints were evaluated on transverse T2-weighted images according to four criteria: (1) the presence of synovial joint fluid, (2) the regularity of the articular surface and presence of subchondral bone sclerosis, (3) the degree of lateral hypertrophic tissue, and (4) the degree of dorsal hypertrophic tissue. The presence of synovial joint fluid was graded zero if the amount of synovial joint fluid was judged to be normal (Fig. 1), one if there was a reduced amount of synovial joint fluid (Fig. 2), and two if the synovial joint fluid signal hyperintensity was completely absent (Figs. 3–5). The regularity of the articular surface and presence of subchondral bone sclerosis was graded zero if the articular surface was smooth with no evidence of subchondral bone sclerosis (Fig 1.), one if it was smooth but with evidence of subchondral bone sclerosis (Figs. 3–5), and two if it was irregular with subchondral sclerosis. The degree of hypertrophic tissue was evaluated over each articular process joint (lateral) and the dorsal lamina (dorsal), and was graded zero if there was a uniform, thin band of hypertrophic material (Fig. 2), one if there was a dense and irregular layer of hypointense tissue covering less than half of the articular process or dorsal lamina, and two if there was a dense and irregular layer of hypointense tissue covering more than half of the articular process or dorsal lamina (Figs. 3–5).

Figure 1.

Transverse T2-weighted MR image of a 9-month-old Great Dane at C3–C4. The articular process joints were normal. Normal synovial fluid signal (arrows) and a smooth appearance of the articular surfaces are evident, with no subchondral bone sclerosis.

Figure 2.

Transverse T2-weighted MR images of a 4-year-old Great Dane with mild articular process degenerative joint disease at C4–C5, oriented cranial (A) to caudal (D). No synovial fluid is evident in B (arrow) but it reappears in C (arrow), suggesting an overall reduction in the amount of synovial fluid. In all other respects the articular process joints appear normal: the articular surfaces are smooth with no evidence of subchondral bone sclerosis, and the cortical bone over the dorsal aspect of the articular processes and the dorsal lamina appears thin and uniform.

Figure 3.

Transverse T2-weighted MRimages of a 4.5-year-old Great Dane with marked articular process degenerative joint disease at C5–C6, oriented cranial (A) to caudal (D). There is a bilateral absence of synovial fluid, with subchondral bone sclerosis (open arrows). Hypertrophic tissue is evident over the right articular process (arrowheads). There is spinal cord compression adjacent to the most severe degenerative changes, with loss of epidural fat, attenuation of the subarachnoid space, and alteration in the shape of the spinal cord on the right and loss of epidural fat on the left.

Figure 4.

Transverse T2-weighted MR images of a 2-year-old Great Dane with dorsal hypertrophic tissue (arrows) at C4–C5, orientated cranial (A) to caudal (D). Adjacent to the hypertrophic tissue there is loss of the epidural fat and attenuation of the subarachnoid space with the spinal cord compression from the dorsal aspect.

Figure 5.

Transverse T2-weighted MR images of a 4-year-old Great Dane with severe articular process degenerative joint disease at C4–C5, orientated cranial (A) to caudal (D). There is a complete absence of synovial fluid, marked subchondral bone sclerosis over the articular process joints, and profuse amounts of hypertrophic tissue over the dorsal aspect of the articular processes and dorsal lamina (arrows). There is loss of epidural fat, attenuation of the subarachnoid space, and severe compression of the dorsal and lateral aspects of the spinal cord.

The degree of spinal cord compression was evaluated on transverse and sagittal T2-weighted MR images and classified as dorsal, lateral (left and right), or disc-associated. If more than one type of spinal cord compression was present, then all types identified were recorded. The degree of vertebral canal stenosis or spinal cord compression was classified as present or absent and then graded as follows: zero: no extension of material into the vertebral canal; 1: reduction or loss of the epidural fat within the vertebral canal without compression of the spinal cord (Fig. 3); 2: attenuation of the subarachnoid space without deviation or distortion of the spinal cord parenchyma (Fig. 3); and 3: compression of the spinal cord with deviation or distortion of the spinal cord parenchyma (Fig. 5). The presence or absence of intramedullary spinal cord change was ascertained using sagittal and transverse T2-weighted MR images and classified as absent if there was no signal hyperintensity and present if there was increased T2-signal in the spinal cord parenchyma. Vertebral foraminal stenosis was evaluated on the transverse T2-weighted MR images at the level of the intervertebral disc and graded as absent if there was no evidence of stenosis and present if stenosis of the vertebral foramina was identified (Fig. 6). Degenerative intervertebral disc changes were evaluated on sagittal plane T2-weighted MR images and graded as absent if there was a homogeneous hyperintense signal and present if there was any loss of the hyperintense signal.

Figure 6.

Transverse T2-weighted MRimage of a 4.5-year-old Great Dane with right foraminal stenosis at C3–C4 (arrow). The articular process joints have a complete absence of synovial fluid, there is bilateral subchondral bone sclerosis which is particularly marked over the right articular process joint, and hypertrophic tissue over both articular processes and the dorsal lamina, but again particularly marked over the right articular process, corresponding with the side of the vertebral foraminal stenosis.

Data were analyzed using commercially available software4. Descriptive statistics for numerical data were reported as mean, median, and range. The frequency of individual degenerative changes within the articular process joints and the frequency of changes that were not related to the articular process joints (spinal cord compression, intramedullary spinal cord changes, intervertebral foraminal stenosis, and intervertebral disc degeneration) were calculated for each cervical intervertebral level. The relationship between the presence of individual articular process joint degenerative changes and the changes that were not related to the articular process joints were examined by calculating the Spearman's rank correlation coefficient with significance defined as P < 0.05. If a positive correlation was found that was interpreted as both variables evaluated increased in severity.

Results

A total of 47 intervertebral spaces and 94 articular process joints were available for analysis: eight articular process joints at C2–C3, 10 at C3–C4, 16 at C4–C5, 20 at C5–C6, 22 at C6–C7, and 18 at C7–T1. Only 13 of 94 (13.8%) articular process joints were normal with all of the dogs showing changes at least in one joint. The highest frequency of degenerative articular process joint changes was in the mid to caudal cervical region (Fig. 7). Loss of the synovial fluid signal and alteration of the articular surfaces were identified most frequently at C4–C5, C5–C6, C6–C7, and C7–T1. Lateral hypertrophy was identified most frequently at C5–C6 and C6–C7 and dorsal hypertrophy at C4–C5 and C5–C6.

Figure 7.

The frequency of individual degenerative changes affecting the cervical articular process joints for each vertebral level. The C2–C3 and C3–C4 vertebral levels had a lower frequency of degenerative changes. The number of dogs assessed at each vertebral level was as follows: C2–C3 (n = 4), C3–C4 (n = 5), C4–C5 (n = 8), C5–C6 (n = 10), C6–C7 (n = 11), and C7–T1 (n = 9).

Loss of the synovial joint fluid was most the frequently identified abnormality in 81 of 94 of articular process joints (86%), followed by loss of regularity of the articular surfaces in 75 of 94 of articular process joints (80%), proliferation of dorsal hypertrophic tissue in 25 of 47 of joints (53%), and proliferation of lateral hypertrophic tissue in 36 of 94 of articular process joints (38%). In all the dogs, loss of the synovial joint fluid and loss of regularity of the articular surfaces was identified in at least one articular process joint and in 11 of the 13 dogs, dorsal or lateral hypertrophic tissue was identified in at least one articular process joint.

Stenosis of the vertebral canal and/or spinal cord compression of varying degrees were identified at 39 of 47 (82.9%) intervertebral spaces and were present in all the dogs (Fig. 8). This varied from reduction or loss of the epidural fat, to reduction or loss of cerebrospinal fluid, to compression of the spinal cord. The most common type of spinal cord compression was lateral, present at 32 intervertebral disc spaces (68.1%) and in 12 of the 13 dogs, followed by dorsal spinal cord compression, present at 23 of 47 (48.9%) intervertebral spaces and 9 of the 13 dogs. In 21 (65.6%) of the intervertebral spaces with lateral spinal cord compression the compression was bilateral (symmetric in 11 [34.4%] and asymmetric in 10 [31.3%]). Disc-associated compression was identified in only seven of the 47 (14.8%) intervertebral spaces and 6 of the 13 dogs.

Figure 8.

The frequency of other changes affecting the cervical vertebral column, besides degenerative changes affecting the articular process joints detailed in Fig. 7, for each vertebral level. The presence of degenerative changes affecting the synovial joint fluid was positively correlated with lateral (P < 0.0001) and ventral (P = 0.0208) spinal cord compression, foraminal stenosis (P = 0.0051), and degenerative intervertebral disc changes (P = 0.0034). The presence of degenerative changes affecting the articular surfaces and lateral hypertrophic tissue were positively correlated with lateral spinal cord compression (P < 0.0001 for both) and foraminal stenosis (P = 0.0001 and P = 0.0002, respectively). The number of dogs assessed at each vertebral level was as follows: C2–C3 (n = 4), C3–C4 (n = 5), C4–C5 (n = 8), C5–C6 (n = 10), C6–C7 (n = 11), and C7–T1 (n = 9).

Lateral spinal cord compression was positively correlated with the presence of degenerative changes affecting the articular synovial fluid (r = 0.4407, P < 0.0001, 95% CI = 0.262 to 0.59), articular surface (r = 0.5814, P < 0.0001, 95% CI = 0.43 to 0.701), and the presence of lateral hypertrophic tissue (r = 0.4865, P < 0.0001, 95% CI = 0.315 to 0.627) with an intermediate strength of correlation, but not with the presence of dorsal hypertrophic tissue (r = 0.1468, P = 0.158, 95% CI = −0.057 to 0.339). However, dorsal hypertrophic tissue was positively correlated with the presence of dorsal spinal cord compression (r = 0.6584, P < 0.0001, 95% CI = 0.526 to 0.759) with an intermediate strength of correlation and negatively correlated with the presence of ventral spinal cord compression (r = –0.2399, P = 0.0198, 95% CI = –0.422 to –0.04) with a weak strength of correlation. Degenerative changes of the articular synovial fluid were positively correlated with ventral spinal cord compression (r = 0.2381, P = 0.0208, 95% CI = 0.038 to 0.42) with a weak strength of correlation.

Intramedullary spinal cord changes were observed in 14 of 47 (29.8%) of the intervertebral spaces examined and 11 of the 13 dogs (Fig. 8). No significant correlation was evident between the presence of individual articular process joint degenerative changes and intramedullary spinal cord changes, including degenerative changes affecting the synovial fluid (r = 0.1537, P = 0.1391, 95% CI = –0.05 to 0.345), articular surface (r = 0.1136, P = 0.2755, 95% CI = −0.091 to 0.309), lateral hypertrophic tissue (r = 0.148, P = 0.1545, 95% CI = −0.056 to 0.34), and dorsal hypertrophic tissue (r = 0.1873, P = 0.0707, 95% CI = −0.015 to 0.375).

Vertebral foraminal stenosis was observed on the right in 12 of 47 (25.5%) and on the left in 7 of 47 (14.9%) of the intervertebral spaces, and in 9 of the 13 dogs (Fig. 8). Vertebral foraminal stenosis was positively correlated with the presence of degenerative changes affecting the articular synovial fluid (r = 0.2868, P = 0.0051, 95% CI = 0.09 to 0.462), articular surface (r = 0.3882, P = 0.0001, 95% CI = 0.202 to 0.547) and the presence of lateral hypertrophic tissue (r = 0.3722, P = 0.0002, 95% CI = 0.184 to 0.534) with a weak strength of correlation, but not with the presence of dorsal hypertrophic tissue (r = 0.112, P = 0.2826, 95% CI = −0.092 to 0.307).

Intervertebral disc changes were observed in 30 of 47 (63.8%) of the intervertebral disc spaces and 12 of the 13 dogs (Fig. 8). Degenerative changes of the intervertebral disc were positively correlated with the presence of degenerative changes affecting the articular synovial fluid (r = 0.2989, P = 0.0034, 95% CI = 0.103 to 0.472) with a weak strength of correlation, but not with degenerative changes affecting the articular surface (r = −0.0491, P = 0.6384, 95% CI = −0.249 to 0.155), or the presence of lateral (r = 0.3722, P = 0.0002, 95% CI = 0.184 to 0.534), or dorsal hypertrophic tissue (r = 0.112, P = 0.2826, 95% CI = −0.092 to 0.307).

Discussion

In this study, 86.2% of the articular process joints had evidence of degenerative changes, consistent with the findings of others.[2, 6, 8, 11] Lateral and dorsal vertebral canal stenosis and/or spinal cord compression were more common than disc-associated vertebral canal stenosis or spinal cord compression, confirming that osseous-associated spinal cord compression is more common in Great Danes dogs.[1, 2, 8, 9, 11] The high frequency of lateral spinal cord compression (68.1%) was similar to that found in a previous computed tomography (CT) myelographic study.[11] The frequency of dorsal compression (48.9%) was similar to a previous MR imaging study (48%) but different to the CT myelography study (8%). This may in part be explained by the greater soft tissue contrast resolution provided by MR imaging than CT myelography.[6, 11] Stenosis was observed in 20% of the intervertebral foramina evaluated and in nine of the 13 dogs (69.2%). These results are similar to the CT myelography study where foraminal stenosis was found in 65.7% of the giant breed dogs.[11] The intervertebral disc level with the highest frequency of articular process joint degenerative changes were C4–C5, C5–C6, C6–C7, and C7–T1 (Fig. 7) and corresponds to the distribution found in pathologic studies.[8, 9] Lateral hypertrophic tissue was identified most frequently at C5–C6 and C6–C7, as reported previously, and dorsal hypertrophy was identified most frequently at C4–C5 and C5–C6.[11] Some have proposed that the degenerative changes evident in the articular process joints may be the consequence of abnormal stresses resulting from abnormal mobility.[2, 9]

We graded individual degenerative changes of the cervical articular process joints, and it proved helpful to investigate the possible association between the presence of these individual articular process joint degenerative changes and the presence of spinal cord compression, foraminal stenosis, intramedullary spinal cord changes, and intervertebral disc degeneration. Similar systems have been used in human patients to evaluate articular process joint changes in the cervical and lumbar region using CT and MR imaging.[12-14] Of the criteria we evaluated, loss of normal synovial fluid was found most frequently and could be a sign of early degenerative changes. Interestingly no dog in this study had articular process joint synovial cysts, as has been found by others in association with degenerative changes of the cervical articular process joints in giant breed dogs.[6, 15]

We found a significant positive correlation between the presence of degenerative changes affecting the articular synovial fluid, articular surface, and lateral hypertrophic tissue and the presence of ipsilateral spinal cord compression and vertebral foraminal stenosis. This suggests that the lateral spinal cord compression and foraminal stenosis seen in Great Dane dogs with cervical spondylomyelopathy may occur secondary to osteoarthrosis affecting the articular process joints or that osteoarthrosis plays a significant role in the pathogenesis of the disease. This is certainly the situation in human patients, where cervical articular process arthrosis is a cause of radiculopathy and sometimes myelopathy.[16, 17] Our results stress the importance of evaluating the articular process joints in Great Dane dogs with evidence of cervical spinal cord disease.

Apart from degenerative changes affecting the synovial fluid, no other significant correlation was evident between individual degenerative changes affecting the articular process joints and the presence of degenerative intervertebral disc changes. This suggests that cervical articular process joint osteoarthritis may precede, or occur independently of, intervertebral disc degeneration in Great Dane dogs. This may also explain the greater frequency of lateral and dorsal spinal cord compression occurring secondary to articular process changes, than disc-associated spinal cord compression. This greater frequency of lateral and dorsolateral spinal cord compressions has also been found in giant breed dogs using CT myelography.[11] This contrasts with the findings in the lumbar spine of human patients, where intervertebral disc degeneration precedes articular process joint osteoarthritis in the lumbar region.[18]

There was a weak positive correlation between the frequency of degenerative changes affecting the articular process joints and the presence of intramedullary spinal cord changes, but this was not statistically significant. One explanation for this is that spinal cord signal change is associated with chronicity, and a number of dogs within this study were less than 2 years of age.

It was not possible to assess all cervical articular process joints in all dogs, as most of the MR imaging studies only included transverse plane images of the region of the vertebral column affected by the most severe spinal cord compression or intramedullary changes. Thus, there could have been a sampling bias with a tendency to include mainly intervertebral spaces with more severe changes.

In conclusion, degenerative changes affecting multiple cervical articular process joints were common in Great Dane dogs affected by cervical spondylomyelopathy. The degenerative changes typically affected multiple articular process joints and were more prevalent in the mid to caudal cervical vertebral column. Degenerative changes affecting the articular process joints frequently coexisted with spinal cord compression and vertebral foraminal stenosis, and in many dogs occurred independent of intervertebral disc degeneration. Assessment of Great Dane dogs with clinical signs suggestive of cervical spondylomyelopathy should include the articular process joints, even if there is no evidence of intervertebral disc degeneration.

  1. 1

    Gyroscan ACS NT, Philips Medical System, Eindhoven, The Netherlands; Magnetom, Siemens, Camberley, UK.

  2. 2

    Magnevist; Bayer HealthCare Pharmaceuticals, UK.

  3. 3

    Osirix Imaging Software, v 3.9.2, Pixmeo, Geneva, Switzerland.

  4. 4

    Minitab 16 Statistical Software, Minitab Inc. State College, PA.

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