Intervertebral disk degeneration is a common disorder in dogs.1–3 In the dog population in Sweden, IVD degeneration—related diseases are among the top 5 reasons for euthanasia of dogs < 10 years old.1,4,5 Intervertebral disk degeneration—related diseases include Hansen type I and II IVD herniation, degenerative lumbosacral stenosis, and cervical spondylomyelopathy.6 Intervertebral disk degeneration is more common in chondrodystrophic breeds than in nonchondrodystrophic breeds and in older dogs than in younger dogs.2,7,8 It is important to mention that IVD degeneration is not synonymous with IVD disease. An IVD that causes clinical signs will invariably be degenerated, but degenerated IVDs are also common findings in dogs without clinical signs of disease.2,9–11
Many similarities exist between IVD degeneration in humans and dogs.7,12–14 For this reason, dogs are sometimes used in research settings as a means to study spontaneous IVD degeneration in humans.15 In humans and dogs, it can be difficult to diagnose IVD degeneration—related diseases, and the use of diagnostic imaging is essential for an accurate diagnosis. It is sometimes difficult to distinguish disks with pathological degeneration from disks that have normal age-related changes (known as normal senile remodeling).16 Moreover, not all degenerated disks cause clinical signs, irrespective of the cause of degeneration.17,18
It is believed that IVD herniation in dogs results from IVD degeneration.7,8 The current surgical treatment is laminectomy in combination with nucleotomy of the herniated disk. However, in humans with IVD degeneration—related diseases, nucleotomy can further destabilize affected vertebrae,19,20 and it is likely that this is also true in dogs.13,14 Although vertebral instability in humans is currently treated by means of vertebral fusion, there is a trend to avoid this type of salvage technique and to focus on regenerative treatment strategies that can be used to achieve functional repair or even regeneration of degenerated IVDs. Such strategies require early identification of the degenerative process through the use of reliable and accurate diagnostic methods and grading systems. Although these types of regenerative treatments may soon be implemented in human medicine, difficulties in identifying early disease in dogs may delay the use of these treatments in veterinary medicine. However, with the rapid development of veterinary diagnostic methods, early treatment to prevent severe clinical signs may soon become available for dogs. Also, when performing clinical research, attempting to stop IVD degeneration, or stimulating IVD regeneration, the Pfirrmann grading scheme is a valuable tool for use in monitoring the progression of degeneration or regeneration of IVDs in vivo.
In human medicine, the Pfirrmann system is the most widely used system for grading IVD degeneration on the basis of MRI findings.21–23 It is based on a system for grading gross pathological changes in IVDs proposed by Thompson et al,24 which is the most commonly used criterion-referenced standard in human medicine. Two systems have been proposed for the grading of IVD degeneration in dogs: use of histologic examination25 and use of gross morphology.26 A third grading system has been proposed for grading of thoracolumbar disks of dogs, but it has not yet been validated.27 None of these systems has been validated for interobserver and intraobserver agreement, nor is there a validated grading system available for IVDs in all locations of the vertebral column.
The purpose of the study reported here was to evaluate whether the MRI-based Pfirrmann system for the grading of IVD degeneration in lumbar disks of humans is applicable for use in all types of dogs and for IVDs in all locations of the vertebral column. Therefore, we determined the interobserver and intraobserver agreement between Pfirrmann scores and evaluated whether biological factors known to increase the extent of IVD degeneration were correlated with higher Pfirrmann scores.7,9
Materials and Methods
Animals—The initial study population was 217 dogs examined at the Clinic of Companion Animals, Utrecht University, The Netherlands, between 2002 and 2008 for which clinicians obtained midsagittal T2-weighted MRI images of any portion of the vertebral column. Although most dogs included in the study were examined because of suspected IVD degeneration—related problems, many were examined for other reasons, such as suspected syringomyelia, neoplasia, fibrocartilaginous emboli, and degenerative myelopathy. Poor image resolution led to the exclusion of data for 15 small-breed dogs. Thus, 994 IVDs from 202 dogs of various breeds and age and both sexes were used for assessment. Of the 202 dogs, 66 were considered (on the basis of breed) to be chondrodystrophic and the remaining 136 were considered to be nonchondrodystrophic. Although there is no comprehensive list of breeds regarded as chondrodystrophic, the Basset Hound, Beagle, Dachshund, Miniature Dachshund, English Bulldog, French Bulldog, Jack Russell Terrier, Pug, Miniature Poodle, Shih Tzu, and Welsh Corgi are typically considered chondrodystrophic breeds.3,6,8,9,27–35 The term IVD degeneration was used to encompass all signs of disk degeneration on MRI images, regardless of the cause of the degeneration and whether the degeneration was associated with clinical signs.
MRI technique—Magnetic resonance imaging was performed by use of a 0.2-T open magnet.a Only T2-weighted MRI images (repetition time, 3,835 to 4,450 milliseconds; echo time, 117 milliseconds) were used. The obtained slices had a thickness of 3 mm. A 21-cm-diameter multipurpose flex coil was used for smaller dogs (dogs fitting the coil), and a circular polarization flexible body and spine coil was used for larger dogs.
Image assessment—The 5-category system developed by Pfirrmann et al23 to grade IVD degeneration in lumbar disks of humans was used (Appendix). Sagittal T2-weighted MRI images were graded separately by 3 observers: a veterinary medical student (observer 1), a student in a PhD program (observer 2), and a board-certified veterinary radiologist (observer 3). The MRI images were examined on standard computer screens by use of software.b Each image depicted a portion of the vertebral column that contained several IVDs. The same disks and sagittal slices were viewed by all observers at the automatic settings provided by the software. All observers were familiar with the Pfirrmann grading procedure and had images with examples of the various grades of degeneration for humans available during the grading procedure. When criteria for > 1 category were applicable to the same IVD, the higher grade was selected because the IVD was considered to have signs of progressive degeneration. The MRI images were graded twice with a 2-week interval between grading for observer 1 and a 6-month interval between grading for observers 2 and 3. Despite the shorter interval for observer 1, bias attributable to recollection of the grade assigned by that reviewer for each of the 994 images was deemed unlikely. Intraobserver agreement of the 3 observers was compared to determine whether the short interval affected grading.
Biological validation—To determine whether results for the Pfirrmann scoring correlated with variables known to be associated with increasing disk degeneration, we evaluated correlations between Pfirrmann scores and each dog's age and predisposition to chondrodystrophy (ie, chondrodystrophic or nonchondrodystrophic breed). Investigators in other studies8,25 have reported that IVD degeneration is strongly correlated with older age and with chondrodystrophic breed. Thus, these variables were used to represent biological validation.
Statistical analysis—Cohen weighted κ analysis was used to evaluate interobserver and intraobserver agreement.36,37 Agreement was interpreted as follows: slight (κ, 0 to 0.20), fair (κ, 0.21 to 0.40), moderate (κ, 0.41 to 0.60), substantial (κ, 0.61 to 0.80), and almost perfect (κ, 0.81 to 1.00).36–38 The mean of the Pfirrmann grades assigned by the 3 observers for each MRI image was calculated, and this mean grade was used to determine whether the degree of degeneration detected on MRI images was correlated with the dog's age or the type of dog (chondrodystrophic or nonchondrodystrophic). A Spearman rank test was used to test for the correlation between age and Pfirrmann grade, and a Mann-Whitney U test was used to test for the association between the type of dog and Pfirrmann grade. Values of P < 0.05 were considered significant.
Results
Animals—Of the 202 dogs, 109 were males and 93 were females. Dogs ranged from 1 to 13 years of age (mean, 5.4 years) and represented 58 breeds. There were IVDs in all regions of the vertebral column (C2–3 disk to L7-S1 disk) included in the study.
IVDs—A total of 994 disks (368 disks from chondrodystrophic dogs and 626 disks from nonchondrodystrophic dogs) were graded on T2-weighted MRI images that each depicted a portion of the vertebral column containing several IVDs (Figure 1). Of the 994 disks evaluated, 265 (26.6%) were assigned a grade of 1, 293 (29.5%) were assigned a grade of 2, and 293 (29.5%) were assigned a grade of 3; only 136 (13.7%) and 7 (0.7%) disks were assigned a grade of 4 and 5, respectively (Figure 2; Table 1). Of the 368 disks from chondrodystrophic dogs, 250 (67.9%) were assigned a grade of 3, 4, or 5. Of the 626 disks from nonchondrodystrophic dogs, 440 (70.3%) were assigned a grade of 1 or 2. In the disks of the chondrodystrophic dogs, Pfirrmann grades 3 and 4 were predominant in dogs > 2 years old (Figure 3), whereas in the nonchondrodystrophic dogs, Pfirrmann grades 1 and 2 were predominant in all age groups. In contrast to other chondrodystrophic dogs, Jack Russell Terriers mainly had IVDs with low Pfirrmann grades, regardless of age of the dog.
A midsagittal T2-weighted MRI image of the cervical portion of the vertebral column of a dog. The C5–6 disk (arrow) has evidence of degeneration (Pfirrmann grade 3).
Citation: American Journal of Veterinary Research 72, 7; 10.2460/ajvr.72.7.893
A midsagittal T2-weighted MRI image of the cervical portion of the vertebral column of a dog. The C5–6 disk (arrow) has evidence of degeneration (Pfirrmann grade 3).
Citation: American Journal of Veterinary Research 72, 7; 10.2460/ajvr.72.7.893
A midsagittal T2-weighted MRI image of the cervical portion of the vertebral column of a dog. The C5–6 disk (arrow) has evidence of degeneration (Pfirrmann grade 3).
Citation: American Journal of Veterinary Research 72, 7; 10.2460/ajvr.72.7.893
A series of midsagittal T2-weighted MRI images of IVDs (arrows) obtained from representative dogs. The images depict Pfirrmann grades of 1 (healthy IVD; far left) to 5 (end-stage IVD degeneration; far right).
Citation: American Journal of Veterinary Research 72, 7; 10.2460/ajvr.72.7.893
A series of midsagittal T2-weighted MRI images of IVDs (arrows) obtained from representative dogs. The images depict Pfirrmann grades of 1 (healthy IVD; far left) to 5 (end-stage IVD degeneration; far right).
Citation: American Journal of Veterinary Research 72, 7; 10.2460/ajvr.72.7.893
A series of midsagittal T2-weighted MRI images of IVDs (arrows) obtained from representative dogs. The images depict Pfirrmann grades of 1 (healthy IVD; far left) to 5 (end-stage IVD degeneration; far right).
Citation: American Journal of Veterinary Research 72, 7; 10.2460/ajvr.72.7.893
Distribution of Pfirrmann grade (1 = light gray bars, 2 = black bars, 3 = white bars, 4 = dark gray bars, and 5 = vertical striped bars) in relation to age in 66 chondrodystrophic dogs (A) and 136 nonchondrodystrophic dogs (B). The number of IVDs per Pfirrmann grade are reported for each age group. In chondrodystrophic dogs, higher Pfirrmann grades predominate in dogs ≥ 2 years old. Grading was performed onT2-weighted MRI images; Pfirrmann scores range from grade 1 (healthy IVD) to 5 (end-stage IVD degeneration).
Citation: American Journal of Veterinary Research 72, 7; 10.2460/ajvr.72.7.893
Distribution of Pfirrmann grade (1 = light gray bars, 2 = black bars, 3 = white bars, 4 = dark gray bars, and 5 = vertical striped bars) in relation to age in 66 chondrodystrophic dogs (A) and 136 nonchondrodystrophic dogs (B). The number of IVDs per Pfirrmann grade are reported for each age group. In chondrodystrophic dogs, higher Pfirrmann grades predominate in dogs ≥ 2 years old. Grading was performed onT2-weighted MRI images; Pfirrmann scores range from grade 1 (healthy IVD) to 5 (end-stage IVD degeneration).
Citation: American Journal of Veterinary Research 72, 7; 10.2460/ajvr.72.7.893
Distribution of Pfirrmann grade (1 = light gray bars, 2 = black bars, 3 = white bars, 4 = dark gray bars, and 5 = vertical striped bars) in relation to age in 66 chondrodystrophic dogs (A) and 136 nonchondrodystrophic dogs (B). The number of IVDs per Pfirrmann grade are reported for each age group. In chondrodystrophic dogs, higher Pfirrmann grades predominate in dogs ≥ 2 years old. Grading was performed onT2-weighted MRI images; Pfirrmann scores range from grade 1 (healthy IVD) to 5 (end-stage IVD degeneration).
Citation: American Journal of Veterinary Research 72, 7; 10.2460/ajvr.72.7.893
Pfirrmann grades for 994 IVDs of 202 chondrodystrophic and nonchondrodystrophic dogs.
| Pfirrmann grade | Nonchondrodystrophic | Chondrodystrophic | Total |
|---|---|---|---|
| 1 | 211 (33.7) | 54 (14.7) | 265 (26.6) |
| 2 | 229 (36.6) | 64 (17.4) | 293 (29.5) |
| 3 | 130 (20.8) | 163 (44.3) | 293 (29.5) |
| 4 | 50 (8.0) | 86 (23.3) | 136 (13.7) |
| 5 | 6 (0.9) | 1 (0.3) | 7 (0.7) |
| Total | 626 (100) | 368 (100) | 994 (100) |
Values reported are the number of IVDs (percentage of total for the column). Grading was perfomed on T2-weighted MRI images; Pfirmann scores ranged from grade 1 (healthy IVD) to 5 (end-stage IVD degeneration).
Intraobserver agreement—Intraobserver agreement was almost perfect (mean ± SE κ, 0.93 ± 0.032, 0.89 ± 0.031, and 0.92 ± 0.032 for observers 1, 2, and 3, respectively; Table 2). In the grades assigned for the 994 IVDs by each of the observers at the 2 grading sessions, there was a difference of 1 grade between scores assigned for 131 (13.2%), 221 (22.2%), and 156 (15.7%) IVDs for observers 1, 2, and 3, respectively. There was a difference of 2 or 3 grades for scores assigned for 20 (2%) of all intraobserver comparisons. No significant difference in intraobserver agreement was detected for the 3 observers.
Intraobserver agreement between 2 grading sessions* and interobserver agreement among 3 observers for assignment of Pfirrmann grades of IVD in 994 MRI images obtained from 202 dogs.
| Comparison | κ (mean ± SE) | No disagreement of grades† | Disagreement of 1 grade† | Disagreement of 2 grades† | Disagreement of 3 grades† |
|---|---|---|---|---|---|
| Intraobserver | |||||
| 1 | 0.93 ± 0.032 | 855 (86.0) | 131 (13.2) | 7 (0.7) | 1 (0.1) |
| 2 | 0.89 ± 0.031 | 763 (76.8) | 221 (22.2) | 10 (1.0) | 0 (0) |
| 3 | 0.92 ± 0.032 | 836 (84.1) | 156 (15.7) | 2 (0.2) | 0 (0) |
| Interobserver | |||||
| 1 and 2 | 0.81 ± 0.030 | 618 (62.2) | 340 (34.2) | 35 (3.5) | 1 (0.1) |
| 1 and 3 | 0.87 ± 0.031 | 720 (72.4) | 263 (26.5) | 11 (1.1) | 0 (0) |
| 2 and 3 | 0.85 ± 0.031 | 669 (67.3) | 322 (32.4) | 3 (0.3) | 0 (0) |
The interval between grading sessions was 2 weeks for observer 1 and 6 months for observers 2 and 3.
Values reported are the number of IVDs (percentage of total IVDs for the row).
Interobserver agreement—Interobserver agreement was almost perfect (mean ± SE κ, 0.81 ± 0.030 between observers 1 and 2, 0.87 ± 0.031 between observers 1 and 3, and 0.85 ± 0.31 between observers 2 and 3; Table 2). For 263 (26.5%) to 340 (34.2%) IVDs, there was a difference of 1 grade between 2 observers. There was a difference of 2 grades between 2 observers for 3 (0.3%) to 35 (3.5%) IVDs, and a difference of 3 grades between observers for 1 (0.1%) image.
Biological validation—A significant association (Z = −10.8; P < 0.001) was detected between Pfirrmann grade and type of dog (chondrodystrophic or nonchondrodystrophic). High grades (ie, more degeneration) were assigned more often for IVDs of chondrodystrophic dogs than for IVDs of nonchondrodystrophic dogs, and low grades (ie, less degeneration) were assigned more often for IVDs of nonchondrodystrophic dogs than for IVDs of chondrodystrophic dogs. In addition, a higher Pfirrmann grade was positively correlated (r = 0.169; P = 0.01) with age of the dog.
Discussion
Use of the Pfirrmann system yielded highly reproducible results for grading IVD degeneration at all vertebral locations in dogs of various breeds and ages. Moreover, the Pfirrmann score was associated with chondrodystrophic breed and age, which are factors associated with IVD degeneration. Thus, the Pfirrmann system would appear to be suitable for use in grading IVD degeneration in dogs.
Of the 994 disks graded, there was perfect agreement between the observers for 618 (62.2%) to 720 (72.4%); for the remaining disks, there was a discrepancy of ≥ 1 grade between the observers. These discrepancies could have resulted from the fact that the Pfirrmann system is not a continuous scale and the cutoff point between 2 categories is not always clear. For example, the discriminating features between grade 1 and 2 (homogeneous vs nonhomogeneous bright signal of the nucleus) and grade 3 and 4 (ability to discriminate between annulus and nucleus) are to some extent subjective, which could explain the reason that 3 (0.3%) to 35 (3.5%) disks had a difference of 2 grades between observers and 1 (0.1%) disk had a difference of 3 grades between observers. In addition, human error, such as viewing the wrong sagittal image during grading or errors when entering IVD grades, is also a potential cause of discrepancies when disks had a difference of 2 or 3 grades.
Although most dogs included in the study were examined because of suspected IVD-related problems, some dogs were examined because of other reasons, which could explain the broad variation in healthy and degenerated disks. Only 7 disks were scored grade 5 (Table 1). It cannot be determined from the present study whether this was representative of end-stage disk degeneration in the canine population. We are not aware of any studies in which investigators examined the association between extent of disk degeneration and severity of clinical signs in dogs. Other studies3,7,8,39,40 have found that chondrodystrophic dogs are more prone to disk degeneration than are nonchondrodystrophic dogs and that older dogs are more likely to have degenerated disks than are younger dogs.
Because the breed standard for the Jack Russell Terrier states that these dogs should have abnormally short limbs in relation to their body length, they were classified as being chondrodystrophic. Surprisingly, most IVDs of the Jack Russell Terriers had low Pfirrmann grades, regardless of age of the dogs. This was in contrast to the higher Pfirrmann grades for the IVDs of the other chondrodystrophic breeds, which suggests that chondrodysplasia causing abnormally short limbs is not necessarily associated with IVD degeneration.
In veterinary medicine, low-field (0.2-T) MRI is generally more available than is high-field MRI. The low resolution of sagittal T2-weighted images with low-field MRI was a problem when viewing the IVDs of miniature breeds, and we had to discard the MRI images of 15 small-breed dogs because of poor image quality. Image resolution provided by use of the low-field MRI was sufficient to provide clear images of IVDs in most dogs, but because the clarity of the images decreased with a decrease in IVD size, it may have been relatively inaccurate for small-breed dogs (the breeds investigated in this study ranged from Bullmastiff to Miniature Dachshund). An additional potential problem was that the coil of the MRI machine provided a limited field of view, which resulted in a brighter signal in the focus area of the magnetic field than in areas of the vertebral column located farther from the coil. This is known as the coil effect, and it can lead to falsely higher Pfirrmann grades for disks located farther from the center of the coil on T2-weighted MRI images.41,42 The T2-weighted MRI images were used for Pfirrmann grading because they best depicted the glycosaminoglycan and water content of disks, which are negatively correlated with the extent of disk degeneration.43,44
The Pfirrmann grading system focuses on characteristic changes in the structure of a disk (T2-weighted signal intensity, disk structure, ability to discriminate between the nucleus and annulus, and disk height) and not on changes in the tissues surrounding each disk (end plate sclerosis, vertebral osteophytes, and disk herniation). However, these aspects in the surrounding tissues should be included to obtain a complete picture of the status of disks. Thus, to obtain accurate information about the extent of potential bulging, protrusion, or extrusion of a disk, transverse and midsagittal (for Pfirrmann grading) MRI images are needed. It has been proposed in 1 study27 that IVD degeneration in the thoracolumbar portion of the vertebral column in dogs can be evaluated on MRI images by the use of 4 criteria: IVD degeneration, bulging of a disk, disk protrusion, and disk extrusion. These basic criteria are also consistent with recommendations made by a joint task force of the North American Spine, Spine Radiology, and Neuroradiology Societies.45 However, to our knowledge, the grading scheme in that aforementioned study27 has not been validated or compared against a criterion-referenced standard. In humans, grading disk degeneration on MRI images by use of the criteria normal, bulging, extrusion, or protrusion has yielded only moderate interobserver agreement.46,47 To accurately evaluate the status of IVDs in dogs, the Pfirrmann grading system should be used in combination with information about disk herniation (if evident), such as protrusion or extrusion, both of which cause stenosis of the vertebral canal.
In the study reported here, interobserver and intraobserver agreement for Pfirrmann grading of IVD degeneration in dogs was almost perfect, with κ scores ranging between 0.81 and 0.93. Moreover, the extent of disk degeneration was significantly associated with breed (chondrodystrophic breeds) and age. On the basis of these results, we conclude that the Pfirrmann grading system can be used to evaluate IVD degeneration in dogs.
ABBREVIATIONS
| IVD | Intervertebral disk |
| MRI | Magnetic resonance imaging |
Magnetom Open Viva, Siemens AG, Munich, Germany.
Web1000 5.1, Clinical Review Station, Agfa Gevaert NV, Mortsel, Belgium.
References
- 1.
Five year statistical report. Stockholm: Agria Insurance, 2000; 33–38.
- 2.
Hoerlein BF. Intervertebral disc protrusions in the dog. I. Incidence and pathological lesions. Am J Vet Res 1953; 14: 260–269.
- 3.
Gage ED. Incidence of clinical disc disease in the dog. J Am Anim Hosp Assoc 1975; 135: 135–138.
- 4.
Egenvall A, Bonnett BN, Olson P, et al. Gender, age, breed and distribution of morbidity and mortality in insured dogs in Sweden during 1995 and 1996. Vet Rec 2000; 146: 519–525.
- 5.
Egenvall A, Bonnett BN, Olson P, et al. Validation of computerized Swedish dog and cat insurance data against veterinary practice records. Prev Vet Med 1998; 36: 51–65.
- 6.↑
Bergknut N. Doctoral thesis. Intervertebral disc degeneration in dogs. Acta Universitatis Agriculturae Sueciae 2010; 91: 19.
- 7.
Hansen HJ. A pathologic-anatomical interpretation of disc degeneration in dogs. Acta Orthop Scand 1951; 20: 280–293.
- 8.
Bray JP, Burbidge HM. The canine intervertebral disk. Part two: degenerative changes—nonchondrodystrophoid versus chondrodystrophoid disks. J Am Anim Hosp Assoc 1998; 34: 135–144.
- 9.
Hansen HJ. A pathologic-anatomical study on disc degeneration in dog, with special reference to the so-called enchondrosis intervertebralis. Acta Orthop Scand Suppl 1952; 11: 1–117.
- 10.
Jones JC, Inzana KD. Subclinical CT abnormalities in the lumbosacral spine of older large-breed dogs. Vet Radiol Ultrasound 2000; 41: 19–26.
- 11.
da Costa RC, Parent JM, Partlow G, et al. Morphologic and morphometric magnetic resonance imaging features of Doberman Pinschers with and without clinical signs of cervical spondylomyelopathy. Am J Vet Res 2006; 67: 1601–1612.
- 12.
Lotz JC. Animal models of intervertebral disc degeneration: lessons learned. Spine 2004; 29: 2742–2750.
- 13.
Bray JP, Burbidge HM. The canine intervertebral disk: part one: structure and function. J Am Anim Hosp Assoc 1998; 34: 55–63.
- 14.
Zimmerman MC, Vuono-Hawkins M, Parsons JR, et al. The mechanical properties of the canine lumbar disc and motion segment. Spine 1992; 17: 213–220.
- 15.↑
Alini M, Eisenstein SM, Ito K, et al. Are animal models useful for studying human disc disorders/degeneration? Eur Spine J 2008; 17: 2–19.
- 16.↑
Adams MA, Roughley PJ. What is intervertebral disc degeneration, and what causes it? Spine 2006; 31: 2151–2161.
- 17.
Bendix T, Kjaer P, Korsholm L. Burned-out discs stop hurting: fact or fiction? Spine 2008; 33: E962–E967.
- 18.
Carragee EJ, Hannibal M. Diagnostic evaluation of low back pain. Orthop Clin North Am 2004; 35: 7–16.
- 19.
Frei H, Oxland TR, Rathonyi GC, et al. The effect of nucleotomy on lumbar spine mechanics in compression and shear loading. Spine 2001; 26: 2080–2089.
- 20.
Zollner J, Heine J, Eysel P. Effect of enucleation on the biomechanical behavior of the lumbar motion segment [in German]. Zentralbl Neurochir 2000; 61: 138–142.
- 21.
Wilke HJ, Rohlmann F, Neidlinger-Wilke C, et al. Validity and interobserver agreement of a new radiographic grading system for intervertebral disc degeneration: part I. Lumbar spine. Eur Spine J 2006; 15: 720–730.
- 22.
Kettler A, Wilke HJ. Review of existing grading systems for cervical or lumbar disc and facet joint degeneration. Eur Spine J 2006; 15: 705–718.
- 23.↑
Pfirrmann CW, Metzdorf A, Zanetti M, et al. Magnetic resonance classification of lumbar intervertebral disc degeneration. Spine 2001; 26: 1873–1878.
- 24.↑
Thompson JP, Pearce RH, Schechter MT, et al. Preliminary evaluation of a scheme for grading the gross morphology of the human intervertebral disc. Spine 1990; 15: 411–415.
- 25.↑
Seiler G, Hani H, Scheidegger J, et al. Staging of lumbar intervertebral disc degeneration in nonchondrodystrophic dogs using low-field magnetic resonance imaging. Vet Radiol Ultrasound 2003; 44: 179–184.
- 26.↑
Sether LA, Nguyen C, Yu SN, et al. Canine intervertebral disks: correlation of anatomy and MR imaging. Radiology 1990; 175: 207–211.
- 27.↑
Besalti O, Pekcan Z, Sirin YS, et al. Magnetic resonance imaging findings in dogs with thoracolumbar intervertebral disk disease: 69 cases (1997–2005). J Am Vet Med Assoc 2006; 228: 902–908.
- 28.
Braund KG, Ghosh P, Taylor TK, et al. Morphological studies of the canine intervertebral disc. The assignment of the Beagle to the achondroplastic classification. Res Vet Sci 1975; 19: 167–172.
- 29.
Goggin JE, Li AS, Franti CE. Canine intervertebral disk disease: characterization by age, sex, breed, and anatomic site of involvement. Am J Vet Res 1970; 31: 1687–1692.
- 30.
Priester WA. Canine intervertebral disc disease—occurrence by age, breed, and sex among 8,117 cases. Theriogenology 1976; 6: 293–303.
- 31.
Brisson BA, Moffatt SL, Swayne SL, et al. Recurrence of thoracolumbar intervertebral disk extrusion in chondrodystrophic dogs after surgical decompression with or without prophylactic fenestration: 265 cases (1995–1999). J Am Vet Med Assoc 2004; 224: 1808–1814.
- 32.
Forterre F, Gorgas D, Dickomeit M, et al. Incidence of spinal compressive lesions in chondrodystrophic dogs with abnormal recovery after hemilaminectomy for treatment of thoracolumbar disc disease: a prospective magnetic resonance imaging study. Vet Surg 2010; 39: 165–172.
- 33.
Eigenmann JE, Amador A, Patterson DF. Insulin-like growth factor I levels in proportionate dogs, chondrodystrophic dogs and in giant dogs. Acta Endocrinol (Copenh) 1988; 118: 105–108.
- 34.
Windsor RC, Vernau KM, Sturges BK, et al. Lumbar cerebrospinal fluid in dogs with type I intervertebral disc herniation. J Vet Intern Med 2008; 22: 954–960.
- 35.
Parker HG, VonHoldt BM, Quignon P, et al. An expressed fgf4 retrogene is associated with breed-defining chondrodysplasia in domestic dogs. Science 2009; 325: 995–998.
- 36.
Landis JR, Koch GG. An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics 1977; 33: 363–374.
- 37.
Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977; 33: 159–174.
- 38.
Koch GG, Landis JR, Freeman JL, et al. A general methodology for the analysis of experiments with repeated measurement of categorical data. Biometrics 1977; 33: 133–158.
- 39.
Ghosh P, Taylor TK, Braund KG. The variation of the glycosaminoglycans of the canine intervertebral disc with ageing. I. Chondrodystrophoid breed. Gerontology 1977; 23: 87–98.
- 40.
Ghosh P, Taylor TK, Braund KG. Variation of the glycosaminoglycans of the intervertebral disc with ageing. II. Non-chondrodystrophoid breed. Gerontology 1977; 23: 99–109.
- 41.
Reicher MA, Gold RH, Halbach VV, et al. MR imaging of the lumbar spine: anatomic correlations and the effects of technical variations. AJR Am J Roentgenol 1986; 147: 891–898.
- 42.
Seeger LL. Physical principles of magnetic resonance imaging. Clin Orthop Relat Res 1989; 244: 7–16.
- 43.
Pearce RH, Thompson JP, Bebault GM, et al. Magnetic resonance imaging reflects the chemical changes of aging degeneration in the human intervertebral disk. J Rheumatol Suppl 1991; 27: 42–43.
- 44.
Benneker LM, Heini PF, Anderson SE, et al. Correlation of radiographic and MRI parameters to morphological and biochemical assessment of intervertebral disc degeneration. Eur Spine J 2005; 14: 27–35.
- 45.↑
Fardon DF, Milette PC. Nomenclature and classification of lumbar disc pathology. Recommendations of the combined task forces of the North American Spine Society, American Society of Spine Radiology, and American Society of Neuroradiology. Spine 2001; 26: E93–E113.
- 46.
Milette PC, Fontaine S, Lepanto L, et al. Differentiating lumbar disc protrusions, disc bulges, and discs with normal contour but abnormal signal intensity. Magnetic resonance imaging with discographic correlations. Spine 1999; 24: 44–53.
- 47.
Brant-Zawadzki MN, Jensen MC, Obuchowski N, et al. Interobserver and intraobserver variability in interpretation of lumbar disc abnormalities. A comparison of two nomenclatures. Spine 1995; 20: 1257–1263.
Appendix
Description of the MRI-based grading system used to classify IVDs in dogs.
| Pfirrmann grade | Structure | Distinction between NP and AF | Signal intensity | Height of IVD |
|---|---|---|---|---|
| 1 | Homogeneous and bright white | Clear | Hyperintense and isointense to CSF | Normal |
| 2 | Nonhomogeneous with or without horizontal bands | Clear | Hyperintense and isointense to CSF | Normal |
| 3 | Nonhomogeneous and gray | Unclear | Intermediate | Normal to slightly decreased |
| 4 | Nonhomogeneous and gray to black | Lost | Intermediate to hypointense | Normal to moderately decreased |
| 5 | Nonhomogeneous and black | Lost | Hypointense | Collapsed disk space |
AF = Annulus fibrosus. NP = Nucleus pulposus.
(Adapted from Pfirrmann CW, Metzdorf A, Zanetti M, et al. Magnetic resonance classification of lumbar intervertebral disk degeneration. Spine 2001;26:1873–1878. Reprinted with permission.)
