Introduction
Thoracolumbar intervertebral disk herniation (TL-IVDH) is the most common cause of neurologic dysfunction in dogs. It is classified into Hansen type I and type II.1 Type I TL-IVDH is observed most often in chondrodystrophic breeds, including Dachshunds, French Bulldogs, and Pekingese.1,2 The disks extrude into the vertebral canal and injure the spinal cord.2 In these breeds, chondroid metaplasia occurs in the nucleus pulposus early in life, and this degenerative process results in calcification of the nucleus pulposus.2,3
Myelography, CT, and MRI are used to diagnose TL-IVDH.4 MRI is considered the gold standard in diagnosis of TL-IVDH, but both low-field and high-field MRI are available in veterinary practices and the quality varies considerably.5,6 Low-field MRI is more common than high-field in Japan, mainly in private practices. In small-breed dogs, it may be difficult to perform diagnostic spine studies with low-field MRI.4 MRI also has lower spatial resolution than CT, which may affect anatomic details.7 CT shows good morphological detail of the spinal cord.7 When combined with myelography, it can also visualize spinal cord compression lesions.
The severity of spinal cord injury is influenced by a variety of factors, including the rate of extrusion and the duration of spinal cord compression.8 Some studies have assessed the correlation between the maximal transverse spinal cord compression ratio and the neurologic severity in dogs with type I TL-IVDH; these studies found that the maximal transverse spinal cord compression ratio is not correlated with neurologic severity.9,10 A different study found a moderate positive correlation between the severity of spinal cord compression and neurologic severity in dogs with cervical spondylomyelopathy.11 None of these studies assessed the volume of compression that might affect neurologic severity, which remains controversial.9–11 In our experience during surgery in dogs with type I TL-IVDH, we sometimes had the impression that a large amount of extruded material was removed compared to the volume of in situ intervertebral disk space, but we know of no studies focusing on the volume of the intervertebral disk. The objective of the study reported here was to assess whether the volume of the extruded materials correlated with neurologic severity in dogs with type I TL-IVDH. We compared the volume of the affected disks with adjacent disks using CT myelographic images of dogs with type I TL-IVDH. We hypothesized that the neurologic severity of type I TL-IVDH would be affected by the volume of the extruded materials.
Materials and Methods
Animals
The medical records database of Nakayama Veterinary Hospital was searched for records of small-breed dogs with type I TL-IVDH diagnosed and surgically treated between July 1, 2016, and June 30, 2018. The identified records were reviewed retrospectively. Dogs were excluded if their records indicated that they had type II TL-IVDH, spinal cord compression lesions that spanned more than 2 vertebrae, or severe spinal cord swelling or if their vertebral CT myelography yielded unclear contrast medium columns evident in the vertebral canal.
Neurologic examination
A neurologic examination was performed on all dogs at the time of admission to the hospital. On the basis of a previous study, all dogs were divided into 5 categories12: grade 1, spinal hyperesthesis only; grade 2, ambulatory paraparesis and ataxia; grade 3, nonambulatory paraparesis; grade 4, paraplegia with intact deep pain sensation; or grade 5, paraplegia with no deep pain sensation.
Diagnostic imaging
After the neurologic examination, we assessed the localization of the affected disk using CT myelography. Myelography was performed by lumbar puncture using iohexol, 240 mg/mL (0.45 mL/kg). All dogs underwent CT imaging (Toshiba Asteion 4 CT scanner; Canon Medical Systems Corp). CT was performed under the following parameters: 120 kV, 150 mA, and 0.5-mm slice thickness. The raw data were reconstructed at a 0.5- to 1.0-mm slice thickness using a bone algorithm with a window width of 2,000 HU and window level of 600 HU.
Surgery and postoperative follow-up
A hemilaminectomy was performed at the site of spinal cord compression, determined by CT myelographic images. In all dogs, the materials extruding into the vertebral canal were removed. Materials included nucleus pulposus, hemorrhage, and torn annulus. The outcome was assessed at the end of the follow-up period by the operating veterinarians or by telephone interviews with the owners or referring veterinarians. The final follow-up physical and neurologic examinations were performed by the operating veterinarians. A successful outcome was defined as follows: grade 1, disappearance of hypersensitivity; grade 2, improvement of ataxia; grades 3 and 4, ambulatory; and grade 5, improvement of deep pain sensation and ambulatory.
Measurement of intervertebral disk volume
The intervertebral disk volume was analyzed using an open-source picture archiving and communication system (PACS) workstation DICOM viewer (OsiriX; Pixmeo SAR). The volume of the disks immediately cranial and caudal to the herniated disk was measured for comparison with the affected disk. The volume of the affected disks was defined as the sum of the volume of the materials that had extruded into the vertebral canal plus the volume of the intervertebral space (Figure 1). The volume of the adjacent intervertebral disks was defined as the volume of the intervertebral space only. The volume of the materials extruded into the vertebral canal was measured by means of a region of interest (ROI).13 The volume of materials was analyzed by manually plotting the ROI using all CT myelography transverse images that showed materials in the vertebral canal. The contours of the ROI defined the outer border of the materials. The volume of the intervertebral space was measured using the ROI.14 The intervertebral space volume was analyzed by manually plotting the ROI using all dorsal plane images of the CT myelography. The contours of the ROI defined the entire invisible space between the cranial and caudal vertebrae. Interpolation of the ROI, between the images with defined ROI, was done automatically by software. The volume of the disks immediately cranial to the herniated disk was an internal control.
Sagittal midline (A), transverse (B through E), and dorsal (F through I) plane CT myelographic images of the vertebral column of a 10-year-old castrated male Miniature Dachshund retrospectively evaluated in a study of 70 small-breed dogs diagnosed with type I thoracolumbar intervertebral disk herniation between July 1, 2016, and June 30, 2018, and evaluated to assess whether the volume of the extruded materials correlated with neurologic severity. The volume of the extruded materials (yellow outlines) and intervertebral space (white outlines) were analyzed. A and F through I—The dog’s head is toward the left (A) or top (F through I). B through I—The dog’s right side is toward the left. The images are displayed in a bone window (window width, 2,000 HU; window level, 600 HU), with a 0.5-mm slice thickness.
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Sagittal midline (A), transverse (B through E), and dorsal (F through I) plane CT myelographic images of the vertebral column of a 10-year-old castrated male Miniature Dachshund retrospectively evaluated in a study of 70 small-breed dogs diagnosed with type I thoracolumbar intervertebral disk herniation between July 1, 2016, and June 30, 2018, and evaluated to assess whether the volume of the extruded materials correlated with neurologic severity. The volume of the extruded materials (yellow outlines) and intervertebral space (white outlines) were analyzed. A and F through I—The dog’s head is toward the left (A) or top (F through I). B through I—The dog’s right side is toward the left. The images are displayed in a bone window (window width, 2,000 HU; window level, 600 HU), with a 0.5-mm slice thickness.
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Sagittal midline (A), transverse (B through E), and dorsal (F through I) plane CT myelographic images of the vertebral column of a 10-year-old castrated male Miniature Dachshund retrospectively evaluated in a study of 70 small-breed dogs diagnosed with type I thoracolumbar intervertebral disk herniation between July 1, 2016, and June 30, 2018, and evaluated to assess whether the volume of the extruded materials correlated with neurologic severity. The volume of the extruded materials (yellow outlines) and intervertebral space (white outlines) were analyzed. A and F through I—The dog’s head is toward the left (A) or top (F through I). B through I—The dog’s right side is toward the left. The images are displayed in a bone window (window width, 2,000 HU; window level, 600 HU), with a 0.5-mm slice thickness.
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Measurement of maximal transverse spinal cord compression ratio
The spinal cord compression ratio was analyzed using an open-source PACS workstation DICOM viewer (OsiriX; Pixmeo SAR). The areas of the maximal transverse compressed spinal cord and transverse uncompressed spinal cord were measured using ROI. The contours of the ROI were defined above the contrast medium. The maximal transverse spinal cord compression ratio was calculated as the area of the transverse vertebral canal minus the area of the maximal transverse compressed spinal cord, divided by the area of the transverse vertebral canal and multiplied by 100.9
Measurement of the disk height index
The disk height index (DHI) is a measure of the ratio of intervertebral disk height to the sum of the height of the 2 adjacent vertebrae (Figure 2).15 The DHI of the affected disks was compared to the DHI of the adjacent disks. An open-source PACS workstation DICOM viewer (OsiriX; Pixmeo SAR) was used to create 3-D multiplanar reconstruction images of the CT myelographic images. The transverse and dorsal plane images were used to adjust the position and depict the midsagittal image of the disk to be measured. By using the midsagittal image of the disk, the DHI was calculated with the following formula: DHI = 2 X (a + b + c) / (d + e + f + g + h + i), where a, b, and c are the dorsal, middle, and ventral intervertebral disk heights, respectively; d, e, and f are the dorsal, middle, and ventral vertebral heights of the cranially adjacent vertebra, respectively; and g, h, and i are the dorsal, middle, and ventral vertebral heights of the caudally adjacent vertebra, respectively.
Sagittal midline plane CT myelographic images of the vertebral column of a 10-year-old castrated male Miniature Dachshund from the study described in Figure 1 showing the locations for measurements to obtain the disk height index with the following formula: 2 X (a + b + c) / (d + e + f + g + h + i). The images are displayed in a bone window (window width, 2,000 HU; window level, 600 HU) with a 0.5-mm slice thickness. Dorsal is toward the top, and the dog’s head is toward the left.
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Sagittal midline plane CT myelographic images of the vertebral column of a 10-year-old castrated male Miniature Dachshund from the study described in Figure 1 showing the locations for measurements to obtain the disk height index with the following formula: 2 X (a + b + c) / (d + e + f + g + h + i). The images are displayed in a bone window (window width, 2,000 HU; window level, 600 HU) with a 0.5-mm slice thickness. Dorsal is toward the top, and the dog’s head is toward the left.
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Sagittal midline plane CT myelographic images of the vertebral column of a 10-year-old castrated male Miniature Dachshund from the study described in Figure 1 showing the locations for measurements to obtain the disk height index with the following formula: 2 X (a + b + c) / (d + e + f + g + h + i). The images are displayed in a bone window (window width, 2,000 HU; window level, 600 HU) with a 0.5-mm slice thickness. Dorsal is toward the top, and the dog’s head is toward the left.
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Statistical analysis
All analyses were performed using statistical analysis software (Prism version 7.0; GraphPad Software; and Statistical Package for Social Sciences, version 29.0, IBM Corporation). Data were evaluated for distribution and variance before election of statistics. The volume of the affected disks and the disks immediately cranial and caudal to the herniated disk was compared using the Friedman test and Dunn multiple comparisons test. The DHI of the affected disks and the cranial or caudal intervertebral disks was compared by the Friedman test and the Dunn multiple comparisons test. The correlation between the volume of the extruded materials and the grade of neurologic severity was analyzed by means of the Kendall rank correlation coefficient. Correlation between the spinal cord compression ratio and the grade of neurologic severity was analyzed by the Kendall rank correlation coefficient. P < .05 was taken as statistically significant. All data were expressed as the mean ± SD. Correlations were classified as follows: < 0.19, very weak correlation; 0.2 to 0.39, weak correlation; 0.4 to 0.59, moderate correlation; 0.6 to 0.79, strong correlation; and > 0.8, very strong correlation.
Results
A total of 90 dogs were diagnosed with type I TL-IVDH, and surgery was performed at the site of spinal cord compression as identified by CT myelography; the extruded materials were surgically removed. Six dogs were excluded from this study because their spinal cord compression lesions extended beyond 2 vertebrae, and 14 dogs were excluded because spinal cord swelling was severe and contrast medium columns were unclear. After that, 70 dogs were eligible for this study. There were 62 Miniature Dachshunds, 2 Toy Poodles, 2 Papillons, 1 French Bulldog, 1 Maltese, 1 Pembroke Welsh Corgi, and 1 mixed-breed dog. The mean age of the dogs was 9.3 years (median, 9.7 years; range, 3 to 16 years), and mean weight was 6.4 kg (median, 6.2 kg; range, 2.8 to 11.4 kg). There were 44 males (63%; 22 were castrated) and 26 females (37%; 13 were spayed). The median number of days from when clinical signs were recognized until surgery was performed was 1 day (range, 0 to 7 days). The grade of neurologic severity was grade 2 in 7 (10%) dogs, grade 3 in 16 (23%) dogs, grade 4 in 28 (40%) dogs and grade 5 in 19 (27%) dogs. Disk herniations were located at T11-12 in 1 dog, T12-13 in 12 dogs, T13-L1 in 16 dogs, L1-2 in 20 dogs, L2-3 in 15 dogs, L3-4 in 5 dogs, and L4-5 in 1 dog.
Sixty-one dogs were followed up by the operating veterinarians. Telephone interviews with the owners (n = 2) or referring veterinarians (7) were performed in 9 dogs. The median follow-up period was 59 days (range, 7 to 180 days). In the grade 2 dogs, 7 dogs had a successful outcome; the success rate was 100% (7/7). In the grade 3 dogs, 16 dogs had a successful outcome; the success rate was 100% (16/16). In grade 4 dogs, 26 dogs had a successful outcome, 1 dog was not ambulatory, and 1 dog ceased deep pain sensation after surgery. The success rate was 93% (26/28). In the grade 5 dogs, 14 dogs had a successful outcome, 1 dog had improvement in deep pain sensation but was not ambulatory, and 4 dogs had no improvement in deep pain sensation. The success rate was 74% (14/19).
The volume of the extruded materials into the vertebral canal was 87.1 ± 66.1 mm3. The volume of the intervertebral space affected was 169.5 ± 61.8 mm3. The total volume of the materials that extruded into the vertebral canal plus the affected intervertebral space was 256.6 ± 112.7 mm3. The volume of the cranial and caudal intervertebral spaces was 165.2 ± 57.1 mm3 and 176.4 ± 61.9 mm3, respectively. The volume of the disks immediately cranial to the herniated disk was 1.0 as an internal control. The total volume of the intervertebral space affected was 1.57 ± 0.42. The volume of the disks immediately caudal to the herniated disk was 1.09 ± 0.22. The total volume of the materials that had extruded into the vertebral canal plus the volume of the affected intervertebral space was significantly larger than the volume of the cranial and caudal intervertebral disks (P < .0001).
The DHI of the affected disks and of the cranial or caudal disks were compared. The DHI of the affected disks, the cranial disks, and the caudal disks were 0.118 ± 0.026, 0.128 ± 0.027, and 0.123 ± 0.026, respectively. The DHI of the affected disks was smaller than that of the cranial disks (P < .001).
The Kendall correlation between the volume of extruded materials or the maximal transverse spinal cord compression ratio and the grades of neurologic severity was assessed. There was a weak positive correlation between the volume of the materials extruded into the vertebral canal and the grade of neurologic severity (r = 0.31; P < .001; Figure 3). There was no correlation between the maximal transverse spinal cord compression ratio and grade of neurologic severity (P = .53; Figure 4).
Scatterplots of the volume of the extruded materials for the dogs described in Figure 1 grouped by grade of preoperative neurologic severity, as follows: grade 1, spinal hyperesthesis only; grade 2, ambulatory paraparesis and ataxia; grade 3, nonambulatory paraparesis; grade 4, paraplegia with intact deep pain sensation; or grade 5, paraplegia with no deep pain sensation. Each circle represents the results for 1 dog. There is a weak positive correlation between the volume of the extruded materials into the vertebral canal and the neurologic severity (r = 0.31; P < .001).
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Scatterplots of the volume of the extruded materials for the dogs described in Figure 1 grouped by grade of preoperative neurologic severity, as follows: grade 1, spinal hyperesthesis only; grade 2, ambulatory paraparesis and ataxia; grade 3, nonambulatory paraparesis; grade 4, paraplegia with intact deep pain sensation; or grade 5, paraplegia with no deep pain sensation. Each circle represents the results for 1 dog. There is a weak positive correlation between the volume of the extruded materials into the vertebral canal and the neurologic severity (r = 0.31; P < .001).
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Scatterplots of the volume of the extruded materials for the dogs described in Figure 1 grouped by grade of preoperative neurologic severity, as follows: grade 1, spinal hyperesthesis only; grade 2, ambulatory paraparesis and ataxia; grade 3, nonambulatory paraparesis; grade 4, paraplegia with intact deep pain sensation; or grade 5, paraplegia with no deep pain sensation. Each circle represents the results for 1 dog. There is a weak positive correlation between the volume of the extruded materials into the vertebral canal and the neurologic severity (r = 0.31; P < .001).
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Scatterplots showing the maximal transverse spinal cord compression ratio and the neurologic severity. Each circle represents the results for 1 dog. No correlation exists between the maximal transverse spinal cord compression ratio and the neurologic severity (P = .53).
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Scatterplots showing the maximal transverse spinal cord compression ratio and the neurologic severity. Each circle represents the results for 1 dog. No correlation exists between the maximal transverse spinal cord compression ratio and the neurologic severity (P = .53).
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Scatterplots showing the maximal transverse spinal cord compression ratio and the neurologic severity. Each circle represents the results for 1 dog. No correlation exists between the maximal transverse spinal cord compression ratio and the neurologic severity (P = .53).
Citation: Journal of the American Veterinary Medical Association 261, 3; 10.2460/javma.22.07.0326
Discussion
In this study, the total volume of the materials that had extruded into the vertebral canal plus the intervertebral space was greater than the volume of the intervertebral disks without herniation according to CT myelographic images. Materials including nucleus pulposus, hemorrhage, and torn annulus could be involved in increasing the volume. There was a weak positive correlation between the volume of the extruded materials at the herniated site and the neurologic severity of type I TL-IVDH by means of the Kendall rank correlation coefficient. We suggest that the volume of extruded materials is at least partly responsible for the presenting neurologic severity in dogs with type I TL-IVDH. There was no correlation, however, between the maximal transverse spinal cord compression ratio and the neurologic severity. Previous studies have found that the maximal transverse spinal cord compression ratio is not correlated with neurologic severity in dogs with type I TL-IVDH on the basis of MRI images.9,10 The extent of compression may exert a greater effect on spinal cord function than the degree of local compression in the spinal cord.10 It is well-known that the interface pressure affects the severity of spinal cord injury and depends on the extent of the extradural lesion.16,17 The severity of spinal cord injury could be influenced by many factors, including the force of the impact, spinal cord displacement, and acceleration.17
There are some findings on radiography that implicate developing herniated disk, including narrowing of the intervertebral space, narrowing of the dorsal articulation, and calcification within the vertebral canal.18 A previous study18 showed that when the intervertebral space is narrowed the positive predictive value is 63% to 71%, indicating that false positives are frequent. In the present study, we have found that there is reduction in the DHI of the affected disks; however, the decrease level is an imperceptible change.
It is known that acute disk herniation can lead to spinal cord swelling.19,20 A previous study21 found that in some dogs the site of spinal cord compression is difficult to identify on myelography because of a filling failure of the contrast medium due to spinal cord swelling. In the present study, broad spinal cord swelling was identified in 14 dogs, in all of which the site of spinal cord compression could be identified, but it was difficult to measure the volume of intervertebral disk herniation.
There were some limitations in the present study including the retrospective study design, the moderate number of dogs included, bias by breed, and the lack of MRI. In the present study, the disks immediately cranial to the herniated disk as a standard was compared to the affected disks. There was a limitation that the current analysis did not allow for confounding variables to be considered, and such variables may have had an important impact on the conclusion reached. Each disk was not individually normalized, so other covariates such as dog breed and weight should be considered. The chondrodystrophy that leads to chondroid metaplasia and degeneration could be affected by all the disks to same degree. What the most stable internal control is for assessment of intervertebral disks needs to be examined. A larger study is also needed to verify the correlation between the volume of the extruded material into the vertebral canal and the grade of neurologic severity.
Acknowledgments
No external funding was involved in this study. The authors declare that there were no conflicts of interest.
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