Cervical disk herniation accounts for almost 21% of all cases of intervertebral disk disease in dogs.1 Despite recent advances in diagnostic imaging modalities, the neurologic examination remains an indispensable part of the diagnosis and localization of cervical disk herniation in dogs.2 Difficulties in determining the neuroanatomic region of cervical disk herniation may be attributable, in part, to the discrepancy in locations of the corresponding intervertebral disks and spinal cord segments. Such discrepancies may be the result of the differing degree of growth of the spinal cord and the vertebral column. Indeed, the vertebral column overgrows the spinal cord in length, and the degree of growth is regionally quite variable. In consequence, 2 spinal cord regions can be distinguished in the cervical vertebral column: an initial cervical region, in which at least the first cervical segment lies within its corresponding vertebra, and a caudal cervical and cranial thoracic region, in which spinal cord segments lie cranial to their corresponding vertebrae.3 Human studies have found that in the cervical spinal cord, the myelomere associated with motor function is shifted by 1 segment and the myelomere associated with sensory function is shifted by 1.5 segments cranial to the corresponding intervertebral level.4 In medium-sized and large dogs, the position of spinal cord segments relative to vertebrae may vary by half a vertebral length cranial or caudal.5 In addition, a laterally herniated C5-C6 disk usually compresses the C6 nerve root, but nerve root compression frequently does not occur with axial disk herniation.
For the purpose of the neurologic examination, the cervical spinal cord may be divided into 2 functional regions: the cranial (C1-C5, UMN) and the caudal (C6-T2, LMN, cervical intumescence) regions. Disk disease affecting the caudal cervical spinal cord region is usually characterized by depressed or absent reflexes, and severe muscle atrophy in the thoracic limbs is only seen in chronic cases of severe myelopathy. Disk disease affecting the cranial spinal cord region is characterized by a range of clinical signs, and reflexes may be normal to exaggerated. Examination of the reflexes of the thoracic limb is therefore vital to determine the site of the cervical disk herniation. However, the extensor carpi radialis, triceps, and biceps reflexes are inconsistent in clinically normal dogs, and examination of reflexes is often limited to the withdrawal (flexor) reflex.6
The purpose of the present study was to evaluate the accuracy of neurologic examination versus MRI in localization of cervical disk herniation and evaluate the usefulness of withdrawal reflex testing in dogs.
Materials and Methods
Case selection—Medical records of client-owned dogs referred for cervical disk herniation between January 2004 and July 2007 were reviewed. Inclusion criteria were that medical records included results of a complete neurologic examination, CBC, serum biochemical profile, MRI examinationa that revealed a single-level lesion, and cervical disk surgery. Dogs were required to be free from orthopedic diseases of the forelimb and have neurologic examination results that indicated a focal cervical lesion.
Clinical examination—Signalment and duration of neurologic dysfunction were taken from the medical record. Acute clinical signs were defined as having occurred < 48 hours before evaluation. The neurologic examination was performed by 1 of 2 board-certified neurologists (AJ, MV). Postural reactions were assessed in all 4 limbs of the standing dog by use of the proprioceptive positioning response (knuckling). Thoracic limbs were palpated for muscle atrophy. Examination of reflexes in the thoracic limbs was based on the withdrawal reflex, which was evaluated by applying a noxious stimulus to the foot while the dog was in lateral recumbency. The least possible stimulus was used, and a hemostat was only used to squeeze a digit when a response could not be elicited by manual squeezing. Flexion of the entire limb, including the shoulder, elbow, and carpal joints, was considered a normal response. If the reflex could only be elicited with a hemostat, it was considered as decreased. Decreased reflexes were interpreted as a sign of lesions in the C6-T2 segments of the spinal cord. The extensor carpi radialis reflex was not used for localization because it is difficult to interpret (an absent or decreased reflex has to be evaluated with caution; strong reflexes are usually exaggerated and indicate a lesion cranial to C7).6 Particular attention was paid to the size of the pupils to detect Horner syndrome (sympathetic tract) and to the cutaneous trunci reflex (lateral thoracic nerve [C8-T1]). Gentle palpation of the cervical muscles was performed to detect cervical spinal hyperesthesia. A lesion was then neuroanatomically attributed to segments C1-C5 (tetraparesis and normal thoracic limb reflex) or C6-T2 (tetraparesis and depressed withdrawal reflexes). Arbitrarily and because of the large anatomic variability at this location,3 it was considered that a lesion localized at the intervertebral disk space C4-C5 (junction between spinal cord regions C1-C5 and C6-T2) might or might not have been responsible for a decreased withdrawal reflex. This decision was based on the idea that localization of a lesion to this transitional site could never be definitively determined because of the variability of spinal cord segments overlying this disk. In the case of a disk herniation at C4-C5, both neurologic localizations (ie, localization to regions C1-C5 and C6-T2) were considered as correct and dogs with this finding were excluded from statistical evaluation of accuracy of localization.
MRI examination—Dogs were premedicated with acepromazine (0.02 mg/kg [0.009 mg/lb], IV) and fentanyl (5 Mg/kg [2.27 Mg/lb], IV). Anesthesia was induced with propofol (4 mg/kg [1.8 mg/lb], IV) and maintained with a continuous rate infusion of fentanyl (5 Mg/kg/h, IV) and inhaled isoflurane (1.5% to 2%) in oxygen. The MRI of the cervical vertebral column was performed in dorsal recumbency. The examinations all included a sagittal and transverse T2-weighted sequence and a dorsal high-resolution T1-weighted sequence. The affected intervertebral disks were assessed for signs of degeneration on mid-sagittal T2weighted images. The severity of spinal cord compression was estimated subjectively by evaluation of the amount of deformation, displacement, and signal intensity changes of the spinal cord. Mild compression was compression of < 25% of spinal cord diameter, moderate compression was compression of 25% to 50% of spinal cord diameter, and severe compression was compression of > 50% of spinal cord diameter. According to the localization of the spinal segments (C1-C5: UMN, C6-T2: LMN), the cervical intervertebral disks were considered cranial (disks C2-C3 and C3-C4) and caudal (disks C5-C6 and C6-C7).
Surgery and follow-up—Surgery was performed immediately after diagnostic imaging. Lactated Ringer's solution (10 mL/kg/h [4.5 mL/lb/h], IV) was administered throughout surgery. Prophylactically, cefazolin (25 mg/kg [11.4 mg/lb], IV) was administered immediately before anesthetic induction and approximately 45 minutes later towards the end of surgery. Monitoring included electrocardiography and measurement of end-tidal CO2 concentrations. All lesions were treated by use of a ventral slot technique.
Dogs were monitored after surgery for signs of pain and functional and neurologic improvement. Pain was assessed via physical examination. Postoperative analgesia was provided with fentanyl (5 Mg/kg/h, IV) for 24 hours, buprenorphine (0.015 mg/kg [0.007 mg/lb], SC, q 8 h) for 3 days, and carprofen (4 mg/kg, PO, once daily) for 1 week. During hospitalization, all dogs underwent postoperative physiotherapy consisting of underwater treadmill training for 10 minutes twice daily and massages and coordination training 5 times daily. Follow-up examinations were performed 6 weeks after surgery. A successful outcome was defined as maintaining or regaining the ability to ambulate unassisted.
Data analysis—Data were analyzed by use of the Fischer exact test to compare the 2 main groups (correct localization of lesion via neurologic examination and incorrect localization via neurologic examination [via comparison with MRI findings]). Influence of body weight (0 to 10 kg [22 lb], > 10 to 20 kg [44 lb], or > 20 kg), age (0 to 5 years, > 5 to 10 years, or > 10 years), sex (male or female), lesion site (C2-C3, C3-C4, C5-C6, or C6-C7), lesion type (acute or chronic), severity of the lesion (signs of pain, ambulatory tetraparesis, or nonambulatory tetraparesis), degree of spinal cord compression (mild, moderate, or severe), and changes in signal intensity of the spinal cord via MRI (normal, slight enhancement, or pronounced enhancement) were statistically tested. Significance was set at P < 0.05.
Results
The 35 dogs included in the study comprised 16 small dogs (< 10 kg), 10 medium-sized dogs (10 to 20 kg), and 9 large dogs (> 20 kg) representing 19 breeds (3 Dalmatians, 1 Rottweiler, 1 Great Dane, 1 Bernese Mountain Dog, 1 Doberman Pinscher, 1 Boxer, 1 German Shepherd Dog, 2 Beagles, 2 Cocker Spaniels, 1 Shar Pei, 5 medium-sized mixed-breed dogs, 4 Dachshunds, 3 Poodles, 2 Yorkshire Terriers, 1 Bichon Frise, 1 Cavalier King Charles Spaniel, 1 West Highland White Terrier, 2 Whippets, and 2 small mixed-breed dogs). Mean age was 7.9 years (median, 7.2 years [range, 2 to 15 years]). Twenty-six (74.2%) dogs were male, and 9 (25.8%) were female.
Association between body weight and results of neurologic examination (black bars = incorrect anatomic localization; white bars = correct anatomic localization) in 26 dogs with single-level cervical intervertebral disk disease.
Citation: Journal of the American Veterinary Medical Association 232, 4; 10.2460/javma.232.4.559
Association between body weight and results of neurologic examination (black bars = incorrect anatomic localization; white bars = correct anatomic localization) in 26 dogs with single-level cervical intervertebral disk disease.
Citation: Journal of the American Veterinary Medical Association 232, 4; 10.2460/javma.232.4.559
Association between body weight and results of neurologic examination (black bars = incorrect anatomic localization; white bars = correct anatomic localization) in 26 dogs with single-level cervical intervertebral disk disease.
Citation: Journal of the American Veterinary Medical Association 232, 4; 10.2460/javma.232.4.559
Distribution of suspected lesion sites as determined via MRI versus neurologic examination in 35 dogs of various breeds with single-level cervical intervertebral disk disease.
Incorrect clinical neuroanatomic localization, as judged by comparison with MRI results, occurred principally (11/14 dogs) with disk herniation that occurred in the cranial cervical vertebral column (C2-C3 or C3C4; Table 1). Errors were less frequently (1/12 dogs) observed in the caudal cervical vertebral column (C5-C6 or C6-C7). Incorrect clinical neuroanatomic localization occurred more frequently in dogs that weighed ≥ 10 kg (P = 0.07; Figure 1). There was no significant (P = 0.39) influence of age or sex on agreement between neurologic and MRI results. Laboratory findings were unremarkable in all dogs. Fifteen (42%) dogs had an acute onset (< 48 hours) of clinical signs, and 20 (58%) were evaluated for chronic signs. Duration of clinical signs was not significantly (P = 0.49) associated with accuracy of clinical neuroanatomic localization. The most common clinical sign was cervical spinal hyperesthesia, which was observed in 88% of dogs (21 dogs had hyperesthesia only, and 10 dogs had hyperesthesia and tetraparesis). Ambulatory tetraparesis was observed in 9 dogs and nonambulatory tetraparesis in 5 dogs. Depressed withdrawal reflex was observed in 30 (85.7%) dogs. Eleven dogs with a depressed withdrawal reflex had a cranial cervical lesion, 11 had a caudal cervical lesion, and 8 had a lesion at intervertebral disk C4-C5. Horner syndrome and changes in cutaneous trunci reflex were not observed in any dogs. Mild muscle atrophy was observed in 9 dogs (1 with a cranial cervical lesion, 4 with a lesion located at C4-C5, and 4 with a caudal cervical lesion) and was associated with a decreased withdrawal reflex in 8 dogs. The severity of clinical signs was not significantly (P = 0.48) associated with agreement between neurologic and MRI diagnoses regarding site of the lesion.
Association between anatomic site of lesion and results of neurologic examination in the same dogs as in Figure 1. See Figure 1 for key.
Citation: Journal of the American Veterinary Medical Association 232, 4; 10.2460/javma.232.4.559
Association between anatomic site of lesion and results of neurologic examination in the same dogs as in Figure 1. See Figure 1 for key.
Citation: Journal of the American Veterinary Medical Association 232, 4; 10.2460/javma.232.4.559
Association between anatomic site of lesion and results of neurologic examination in the same dogs as in Figure 1. See Figure 1 for key.
Citation: Journal of the American Veterinary Medical Association 232, 4; 10.2460/javma.232.4.559
Association between degree of spinal cord compression and results of neurologic examination in the same dogs as in Figure 1. See Figure 1 for key.
Citation: Journal of the American Veterinary Medical Association 232, 4; 10.2460/javma.232.4.559
Association between degree of spinal cord compression and results of neurologic examination in the same dogs as in Figure 1. See Figure 1 for key.
Citation: Journal of the American Veterinary Medical Association 232, 4; 10.2460/javma.232.4.559
Association between degree of spinal cord compression and results of neurologic examination in the same dogs as in Figure 1. See Figure 1 for key.
Citation: Journal of the American Veterinary Medical Association 232, 4; 10.2460/javma.232.4.559
The most common sites of lesions as detected via MRI were the intervertebral disk spaces at C2 to C3 (9 dogs) and C4 to C5 (9 dogs). Incorrect neurologic localization based on a depressed withdrawal reflex was significantly (P < 0.001) associated with lesions of the cranial cervical vertebral column (11/14 dogs; Figure 2). A depressed withdrawal reflex was detected in 11 of 12 dogs with caudal cervical disk herniation. Signal intensity changes of the spinal cord on MRI were not significantly (P = 0.49) associated with the rate of agreement between diagnostic methods. Severe spinal cord compression was not significantly (P = 0.09) associated with a higher rate of incorrect neurologic localization (Figure 3).
Overall, 32 (91%) dogs had a successful surgical outcome. Twenty-three dogs, of which 19 had depression of the withdrawal reflex before surgery, were assessed neurologically 6 weeks after surgery. Of those 19 dogs, depression of the withdrawal reflex persisted in 6 dogs and a normal reflex was observed in the remaining 13.
Discussion
Cervical intervertebral disk herniation is a relatively common (6% of neurologic diseases) neurologic disease in dogs in our referral institution.1 The Dachshund and Beagle have been described as the breeds most commonly affected.7 In the present study, 19 breeds of dogs were represented. Dachshunds were among the most common small dogs and Dalmatians were among the most common large dogs affected. Mean age of affected dogs was 7.9 years, which is consistent with previous reports.7,8 An acute onset of clinical signs was observed in 42% of dogs, which is also consistent with a previous report.9
Magnetic resonance imaging is a useful tool in the evaluation and diagnosis of canine cervical intervertebral disk disease.10 Disk herniation and spinal cord compression were best recognized by a loss of epidural fat and a change in the shape of the spinal cord on the transverse images. One limitation of the study may have been the lack of CSF examination because this would have permitted meningomyelitis and secondary incidental disk herniation to be definitively ruled out. However, undiagnosed meningomyelitis is unlikely because this is uncommon and all dogs improved clinically following surgery. The most common sites of disk herniation in the present study were C2-C3 and C4-C5. This is in agreement with previous studies8,9,11 in which the most common site reported was C2-C3. The most common clinical sign in the dogs in the present study was cervical spinal hyperesthesia. The location of herniated disk fragments within the vertebral canal is the most important factor in determining whether affected dogs have hyperesthesia or tetraparesis.8,11 If disk material herniates in a dorsolateral direction, nerve root compression and pain occur. However, if disk material herniates toward the midline, it is more likely to cause spinal cord compression and subsequent ambulatory or nonambulatory tetraparesis, as was evident in 9 and 5 dogs, respectively. A depressed withdrawal reflex was seen in 30 dogs. In 19 dogs, this finding could be explained by extruded intervertebral disk material compressing the spinal cord or nerve root at the level of the cervical intumescence. In the 11 remaining dogs in which a cranial cervical lesion (C2-C3 or C3-C4) was diagnosed with MRI, the depressed reflex could not be explained by any degree of disparate growth between the spinal cord and the vertebral column and other explanations must be sought.
Withdrawal reflexes are tailored to produce the most appropriate movement according to the site at which the stimulus is applied, which could require extensors to act as the primary movers.12 The reflex varies as a function of the stimulation site.13,14 the position of the limb,15 the load applied to the limb,16 and the stimulation intensity.12,17 In the present study, the neurologic examination was performed in a standardized manner, so interobserver variation in technique was unlikely. It is, however, still possible that slight variations in technique may have resulted in reflex responses that influenced the assessment of lesion localization. In a previous study18 of withdrawal reflexes in the upper limb in humans, a previous stimulus did not influence the physiologic reaction or subjective sensations but the possibility of slow habituation over time could not be excluded. Reflexes were only repeated 2 to 3 times during the examination of dogs in the present study, so habituation was also unlikely to cause depression of the reflex. Individual differences in anxiety levels have not been found to affect the threshold level determining the withdrawal reflex, 19 although a small dog that is stressed and difficult to position may be difficult to examine and the interpretation of the withdrawal reflex may be more difficult than in a large-breed quiet dog that is well positioned. In chronic cases, the withdrawal response may be altered by uneven muscle atrophy, absence of descending central nervous stimuli on the spinal cord, or changes within the flexion pathways of the spinal cord circuitry.20 Muscle atrophy influences the contractile properties of the muscles in a negative fashion and may alter the flexor reflex response. However, severe muscle atrophy was not a consistent finding in dogs in the present study and could not have been the cause of a depressed reflex in 9 dogs with cranial cervical lesions. A depressed reflex and mild muscle atrophy were only evident in 1 of 11 dogs with cranial cervical disk herniation. A change in the functional organization of the withdrawal reflex pathways because of loss of descending stimuli on the spinal cord cannot be ruled out as an explanation for the depressed reflex observed in dogs with a lesion from C1 to C4. Indeed, a number of excitatory and inhibitory supraspinal inputs including the corticospinal,21 rubrospinal,22 vestibulospinal,23 and medullary reticulospinal tracts24 influence the pathways of the withdrawal reflex. Moreover, other spinal reflex circuits, modified as a result of injury, may also influence the functional organization of the withdrawal reflex through interneural connections. The long-term loss of descending input to the spinal cord may also result in neuroplastic changes within the withdrawal reflex circuitry. Results of a previous study25 of the modifying effects of locomotor training on patients with chronic spinal cord injury that was classified as clinically complete suggest that neuroplasticity can occur in the spinal pathways in chronic spinal cord injury. Incorporating the flexor reflex to assist the swing phase of locomotion during training further improves kinematics during locomotion.26
In humans, the agreement of lesion localization between the neurologic examination and MRI findings decreases as patient age increases. Factors that may attribute to this finding include a general decrease in reflex and muscle strength with advancing age, which hampers results of the neurologic examination, and complication associated with other diseases such as degenerative myelopathy in elderly human patients.27 Age did not seem to be associated with errors in neurologic localization in the present study. However, this result should be interpreted cautiously because few dogs varied widely in age.
Results of the present study suggested that neurologic examination is frequently inaccurate as a method of preoperative neuroanatomic localization of cervical disk herniation in dogs and error is most likely to occur in dogs with lesions from C2 to C4. One clinical implication of this observation may be that MRI examinations, which are used more frequently now for diagnosis of spinal cord diseases, should not only focus on a small restricted area defined by the neurologic examination.
ABBREVIATIONS
| UMN | Upper motor neuron |
| LMN | Lower motor neuron |
| MRI | Magnetic resonance imaging |
Hitachi Airis II, 0.3 Tesla, Hitachi Medical Systems, Düsseldorf, Germany.
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