In dogs, CSM, also called wobbler syndrome, can affect the cervical portion of the vertebral column causing compression of the spinal cord, spinal nerve roots, or both.1,2 There are 2 forms of CSM, which may develop separately or in conjunction.1 Disk-associated CSM results from spinal cord compression secondary to intervertebral disk protrusion and usually develops in large-breed dogs.3 Osseous-associated CSM more commonly affects giant breeds, with compression of the spinal cord resulting mainly from osseous proliferation of the articular processes.4,5 Hypertrophy of the ligamenta flava may also be present with either form of CSM.6 The breeds that most commonly develop the disk-associated and osseous-associated forms of CSM are Doberman Pinscher and Great Dane, respectively.6–11 There are few reports6,8,10–13 of CSM in German Shepherd Dogs, with correspondingly few descriptions of the neurologic and MRI features of the disease in this breed.
German Shepherd Dogs are predisposed to many orthopedic diseases (primarily hip dysplasia and elbow dysplasia14) and vertebral and spinal cord disorders (eg, degenerative myelopathy, degenerative lumbosacral stenosis, and cranial thoracic intervertebral disk herniation15–17). Cervical spondylomyelopathy is an uncommon differential diagnosis for a German Shepherd Dog with signs of a cervical myelopathy. Over the past few years, we have identified several German Shepherd Dogs with CSM, for which CSM often was not initially considered as a differential diagnosis. The objective of the study reported here was to describe the neurologic signs and MRI findings in a group of German Shepherd Dogs with CSM. Through the description of these features of CSM, we hope to raise awareness of the importance of CSM as a differential diagnosis for German Shepherd Dogs with signs of cervical myelopathy.
Materials and Methods
Case selection criteria
For this retrospective case series, medical and imaging records were searched to identify all dogs with a confirmed diagnosis of CSM (on the basis of clinical signs and MRI features) from January 2006 through July 2018 at The Ohio State University Veterinary Medical Center. Dogs were included in the study on the basis of breed (German Shepherd Dogs) and the availability for review of medical record data (ie, signalment, history, diagnosis, results of neurologic examination, treatment, and outcome) and MRI images obtained at the time of diagnosis.
Medical records review
The following data were obtained from each dog's medical record: age, duration of clinical signs, presence of neurologic signs (eg, ataxia or cervical hyperesthesia), and treatments administered. Outcome information was obtained from medical records or via telephone conversations with the owners. The CSM was classified as acute when signs developed suddenly (< 1 week before diagnosis) and as chronic when signs developed more slowly (≥ 1 week before diagnosis).
Magnetic resonance imaging was performed with a 3.0-T MRI scanner; although protocols varied, sagittal T1-weighted and T2-weighted images of the C2 through T1 vertebrae and transverse T1-weighted and T2-weighted images of the sites of spinal cord compression were available for each dog. Sagittal and transverse MRI images were evaluated by a board-certified veterinary neurologist (RCdC), and information recorded included the cause and main site of spinal cord compression and the presence of osseous proliferation of the articular processes or laminae; intervertebral disk protrusion, extrusion, or degeneration; intervertebral foraminal stenosis; and spinal cord signal changes (hyperintensity on T2-weighted MRI images, with or without hypointensity on T1-weighted images, compared with normal spinal cord parenchyma).
Compression of the spinal cord was classified as mild, moderate, or severe (ie, compression was < 25%, 25% to 50%, and > 50%, respectively, relative to cross-sectional area of immediately adjacent [cranially or caudally] noncompressed spinal cord).3,5 The main site of spinal cord compression was identified as the site with the greatest spinal cord compression (on the basis of cross-sectional area) and T2-weighted hyperintensity (when present). On transverse MRI images, intervertebral foraminal stenosis was identified as a reduction of > 25% in the expected diameter of the intervertebral foramen at mid-distance between the adjacent vertebral endplates.3,5
Intervertebral disk protrusion and extrusion were differentiated according to previously published guidelines.18 Intervertebral disk protrusion was considered to be present when there was midline instead of lateralized intervertebral disk herniation and partial instead of complete intervertebral disk degeneration. Intervertebral disk degeneration was characterized as a loss of the normal T2-weighted hyperintensity of the nucleus pulposus, regardless of bulging of the disk.7
When available, radiographs and CT images were also evaluated for osseous changes in the articular processes or laminae. One dog also underwent kinematic MRI, which included collection of sagittal and transverse T2-weighted images obtained during flexion and extension of the neck; although these images were evaluated, only conventional images obtained with the neck in a neutral position were used for classification of lesions, to ensure that all cases were evaluated in a consistent manner.
Results
Among 129 dogs identified with a confirmed diagnosis of CSM within the study period, 10 (7.8%) were German Shepherd Dogs. There were 8 castrated and 1 sexually intact males and 1 spayed female; the mean and median age of the dogs was 6.2 and 6 years, respectively (6 dogs were 6 to 12 years old, 3 dogs were 2 to < 6 years old, and 1 dog was 1.5 years old). On the basis of the duration of clinical signs, 9 dogs were classified as having chronic CSM (duration range, 3 weeks to 8 months), and 1 dog (a castrated male) was classified as having acute CSM.
For 4 of the 9 dogs with chronic CSM, the initial diagnostic efforts of the referring veterinarians focused on the thoracolumbar and lumbosacral portions of the vertebral column because forelimb involvement was not identified at the time. In these 4 dogs, the clinical signs of CSM were initially attributed to 1 or more other conditions that were also present (lumbosacral stenosis [n = 4], thoracolumbar or lumbosacral intervertebral disk protrusion [2], and osteoarthritis of the hip joint [1]). Altogether, 7 of the 10 German Shepherd Dogs had concurrent conditions (orthopedic or neurologic conditions or both) present at the time of CSM diagnosis; concurrent conditions included lumbosacral stenosis (n = 5), thoracolumbar or lumbosacral intervertebral disk protrusion (4), cranial cruciate ligament rupture (2), and osteoarthritis of the hip joint (1).
On neurologic examination, all 10 dogs were ambulatory, and 9 of the 10 dogs had proprioceptive ataxia that was often more severe in the hind limbs than the forelimbs; 3 dogs were noted to have a 2-engine gait (ie, forelimb strides were shorter than hind limb strides). Three of the 10 dogs had signs of cervical hyperesthesia, which was the only clinical sign in only 1 dog. Among the 10 dogs, the examination findings included decreased flexor reflex and extensor tone in the forelimbs with normal flexor and patellar reflexes in the hind limbs (n = 5), increased extensor tone in all 4 limbs with decreased flexor reflex in the forelimbs (3), and increased extensor tone and normal flexor reflexes in the forelimbs with normal flexor and patellar reflexes in the hind limbs (2); these findings corresponded with neuroanatomic localization of a myelopathy within the spinal cord segments at C6-T2, C6-C8, and C1-C5, respectively.
For 7 dogs, cervical radiographic views were available for examination, which revealed osseous proliferation at the articular processes in all 7 dogs (total of 15 affected sites) and sclerosis and thickening of the vertebral laminae (characterized by increased radiopacity; total of 7 affected sites) in 2 dogs (Figure 1). Computed tomography, performed for 4 dogs, revealed primarily osseous proliferation of the articular facets and occasional osseous proliferation of the laminae with resultant stenosis of the vertebral canal (Figure 2). Among those 4 dogs, bilateral osseous proliferation of the articular processes with variable degrees of subchondral sclerosis was observed at 13 intervertebral sites: C5-6 (n = 4 dogs), C6-7 (3), C4-5 (3), and C3-4 (3). Thickening of the laminae was observed at 8 intervertebral sites: C3-4 (n = 3 dogs), C5-6 (3), C4-5 (1), and C6-7 (1).
Among the 10 dogs, MRI images revealed that the main site of spinal cord compression was at the C6-7 (n = 5), C5-6 (4), or C4-5 (1) intervertebral space. Spinal cord compression at these sites was caused exclusively by osseous proliferation of the articular processes (n = 5 dogs), hypertrophy of the ligamenta flava and thickening of the dorsal laminae (2), or a combination of causes (ligamenta flava hypertrophy and osseous proliferation of the articular processes; ligamenta flava hypertrophy and intervertebral disk protrusion; or intervertebral disk protrusion, vertebral body tipping, and ligamenta flava hypertrophy [1 each]). The main spinal cord compressions were classified as severe (n = 5 dogs), moderate (2), or mild (3).
Nine of the 10 dogs had osseous proliferation of the articular processes that caused various degrees of spinal cord compression at 11 intervertebral sites (C6-7 [n = 5 dogs], C5-6 [4], and C4-5 [2]). Eight of the 10 dogs had hypertrophy of the ligamenta flava that caused various degrees of spinal cord compression at 16 intervertebral sites (C5-6 [n = 8 dogs], C4-5 [7], and C1-2 [1]; Figures 2–4).
Spinal cord hyperintensity at sites of spinal cord compression was observed on T2-weighted MRI images obtained from 9 of the 10 dogs; 2 of these dogs had a corresponding hypointensity on T1-weighted MRI images at sites where spinal cord compression was caused by bilateral osseous proliferation of articular processes or ligamenta flava hypertrophy and laminae thickening. Spinal cord hyperintensity associated with spinal cord compression of various causes was observed at 11 intervertebral sites: C6-7 (from osseous proliferation of articular processes [n = 5 dogs]); C5-6 (from osseous proliferation of articular processes and ligamenta flava hypertrophy [2], ligamenta flava hypertrophy [1], and ligamenta flava hypertrophy with laminae thickening and intervertebral disk protrusion [1]); C4-5 (from ligamenta flava hypertrophy and laminae thickening [1]); and C3-4 (from ligamenta flava hypertrophy with laminae thickening and osseous proliferation of the articular processes [1]). Two dogs each had 2 sites of spinal cord hyperintensity that corresponded with spinal cord compression at the C6-7 (as a result of osseous proliferation of the articular processes) and C5-6 (as a result of osseous proliferation of the articular processes and ligamenta flava hypertrophy) intervertebral spaces (Figure 3).
All 10 dogs had some degree of intervertebral foraminal stenosis (unilateral or bilateral), with 30 affected sites (C5-6 [n = 9 dogs], C6-7 [8], C4-5 [7], C3-4 [4], and C7-T1 [2]. Five of 10 dogs had some degree of intervertebral disk protrusion, with 8 disks affected (Figure 4); 9 of 10 dogs had some degree of intervertebral disk degeneration, with 23 disks affected. Additionally, an extradural synovial cyst within the vertebral canal was observed on T2-weighted MRI images for each of 3 dogs (at the C6-7 [n = 2] and C5-6 [1] intervertebral spaces).
For the dog that underwent kinematic MRI, extension of the neck resulted in worsening of the spinal cord compressions that were present at 2 intervertebral spaces (C5-6 [caused by intervertebral disk protrusion, vertebral body tipping, and ligamenta flava hypertrophy] and C5-7 [caused by osseous proliferation of the articular processes]), compared with the degree of spinal cord compression with the neck in the neutral position. On flexion of the neck, the spinal cord compression at both sites was less severe than that observed with the neck in the neutral position.
For the 10 dogs, information on outcomes following medical treatment or surgery was obtained from medical records (n = 2) and via telephone conversations with the owners (8). Two dogs underwent surgical procedures (intervertebral arthrodesis with bone grafting [C6-C7; n = 1] and dorsal laminectomy [from C5 through C7; 1]). The dog that underwent arthrodesis had initial worsening of clinical signs, which subsequently improved, but was euthanized 1.3 years after surgery because of eventual worsening of clinical signs. The dog that underwent dorsal laminectomy also had initial worsening of clinical signs with subsequent improvement, and its condition was stable for 3 years after surgery; this dog was euthanized at 4 years after surgery because of progressive worsening of clinical signs. Eight dogs received medical management: 4 dogs were administered prednisone or dexamethasone long term, 2 dogs were mainly administered meloxicam long term (1 dog was temporarily switched to prednisone treatment on 2 occasions when there was worsening of clinical signs; meloxicam administration was resumed after improvement of clinical signs), 1 dog was administered carprofen and gabapentin (as needed) long term, and 1 dog was administered prednisone for 1 month and gabapentin long term. Among the 8 medically managed dogs, 5 had initial improvement of clinical signs but then subsequent progression of the disease and worsening of clinical signs (these dogs were euthanized a mean of 1.2 years after diagnosis [median, 1.3 years; range, 0.3 to 1.7 years]), 1 dog had periods of worsening clinical signs but was reportedly in stable condition during the last year of life and died of unrelated illness, and 2 dogs were alive at the time of last follow-up (the dog that was administered only carprofen and gabapentin was clinically stable at 3.3 years after diagnosis, and the dog that was administered prednisone and gabapentin had improvement of clinical signs and was clinically stable at 2.5 months after diagnosis). Mean and median survival times for the 8 nonsurviving dogs were 2.18 and 1.5 years, respectively.
Discussion
In the present report, the neurologic and MRI features of German Shepherd Dogs with CSM have been described. Previously, CSM had been reported6,11,12 for only a few German Shepherd Dogs from the United States. The German Shepherd Dogs with CSM seen at our veterinary medical center in recent years has highlighted the importance of including CSM as a differential diagnosis for German Shepherd Dogs with neurologic signs and signs of cervical hyperesthesia.
The results of the present study indicated that German Shepherd Dogs have a greater prevalence of hypertrophy of the ligamenta flava associated with osseous proliferation of the articular processes than other breeds.4,5,8 Eight of the 10 German Shepherd Dogs included in the present study had spinal cord compression that was predominately associated with osseous proliferation of the articular processes but also included hypertrophy of the ligamenta flava as a contributing component. To our knowledge, such a high proportion of dogs with a ligamentous component in osseous-associated CSM has not been previously reported for any dog breed.5,6,10,19,20
The German Shepherd Dogs of the present study were older than dogs of other breeds with osseous-associated CSM (eg, Great Dane and Mastiff) in other reports.5,6 Among the dogs of the present study, the duration of clinical signs prior to diagnosis was approximately 5 months, but it is possible that mild signs were incorrectly interpreted or went unnoticed in dogs with concurrent orthopedic issues. Indeed, for 4 dogs, forelimb involvement was not initially identified, and the clinical signs of cervical myelopathy were attributed to 1 or more other conditions that were also present (ie, lumbosacral stenosis, osteoarthritis of the hip joint, and thoracolumbar or lumbosacral intervertebral disk protrusion).
Although German Shepherd Dogs are considered to be at a risk for disk protrusion in the cranial thoracic region of the vertebral column because of the large number of degenerated disks,17 we observed only a small number of disk protrusions on available images from the dogs of the present study. However, because the MRI images for the dogs of present study were mainly of the cervical vertebral region, only part of the cranial thoracic vertebral region was evaluated.
Great Danes and Doberman Pinschers make up approximately 60% to 70% of all CSM cases in dogs,6–11 but this condition has also been described for other breeds (eg, Mastiff,6 Boerboel,20 and Bernese Mountain Dog19). The hypertrophy of the ligamenta flava noted in the German Shepherd Dogs of the present study was similar to the soft tissue appearance associated with a vertebral arch anomaly reported in a case series21 of 18 Basset Hounds; however, only 1 of the Basset Hounds described in that report21 had involvement of the articular processes, whereas all the German Shepherd Dogs of the present report had some degree of articular process degeneration or proliferation (or both), and only 2 had dorsal laminae thickening and osseous proliferation into the vertebral canal.
It is also important to note that several of the MRI features (eg, spinal cord compression caused by osseous proliferation of the articular processes) were only observed on transverse images and not on sagittal images, highlighting the importance of routine acquisition of transverse sections of at least the caudal cervical intervertebral spaces (C4-5, C5-6, and C6-7) and possibly of all cervical intervertebral spaces. Also, because the osseous form of CSM is usually a multifocal disease, it is important to evaluate the entire cervical portion of the vertebral column if 1 lesion is found and to include both T2- and T1-weighted MRI images in the sagittal and transverse planes to allow detection of ligamentous and osseous changes.
For dogs with neurologic signs localized to the cervical region, CSM should be included in the list of differential diagnoses along with neoplasia, intervertebral disk herniation, subarachnoid diverticulum, and vertebral synovial cyst. Although localization of a lesion to the cervical portion of the spinal cord will help to exclude other common neurologic diseases (eg, degenerative myelopathy, thoracolumbar intervertebral disk disease, and degenerative lumbosacral stenosis14–17,22), dogs with CSM or other causes of cervical myelopathy may initially only have obvious clinical signs in the hind limbs.
All 5 dogs with compression of the spinal cord that was classified as severe had spinal cord signal changes at the main site of compression; 2 of these dogs also had hypointensity at corresponding sites of spinal cord compression on T1-weighted MRI images, a sign generally associated with irreversible spinal cord injury and a poorer prognosis.23 However, because only 2 dogs in the present study had this MRI finding, we were unable to draw any conclusions from these cases. Kinematic MRI can potentially provide additional information regarding spinal cord compression beyond that provided by MRI of animals during neutral positioning of the neck, such as identification of additional sites of compression or changes in compression associated with flexion or extension of the neck,24 as was observed in the 1 dog of the present study that underwent kinematic MRI.
In the present report, the small number of dogs, only 2 of which underwent surgical treatment, precluded us from drawing conclusions about treatment effectiveness and prognosis. Another limitation was that follow-up information for most dogs was obtained via telephone contact with the owners, and because of the time that had passed, detailed information regarding administered medications (ie, frequency of administration and dose) was not available. Among the German Shepherd Dogs with osseous-associated CSM included in the present study, most had ligamenta flava hypertrophy as a component of the disease process. Most dogs were > 5 years of age and had a history that indicated the CSM was chronic and progressive. Diagnosis of CSM in German Shepherd Dogs can be difficult because of concurrent orthopedic or other neurologic diseases. Cervical spondylomyelopathy should be considered as a differential diagnosis in German Shepherd Dogs with neurologic signs of ataxia or paresis or signs of cervical hyperesthesia.
Acknowledgments
No external funding was used in this study. The authors declare that there were no conflicts of interest.
ABBREVIATIONS
CSM | Cervical spondylomyelopathy |
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