Reliability of macroscopic grading of intervertebral disk degeneration in dogs by use of the Thompson system and comparison with low-field magnetic resonance imaging findings

Niklas Bergknut Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, Utrecht University, 3508 TD Utrecht, The Netherlands.

Search for other papers by Niklas Bergknut in
Current site
Google Scholar
PubMed
Close
 DVM, PhD
,
Guy Grinwis Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, 3508 TD Utrecht, The Netherlands.

Search for other papers by Guy Grinwis in
Current site
Google Scholar
PubMed
Close
 DVM, PhD
,
Emile Pickee Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, Utrecht University, 3508 TD Utrecht, The Netherlands.

Search for other papers by Emile Pickee in
Current site
Google Scholar
PubMed
Close
 BSc
,
Edoardo Auriemma Division of Diagnostic Imaging, Faculty of Veterinary Medicine, Utrecht University, 3508 TD Utrecht, The Netherlands.

Search for other papers by Edoardo Auriemma in
Current site
Google Scholar
PubMed
Close
 DVM
,
Anne-Sofie Lagerstedt Department of Clinical Sciences, Faculty of Veterinary Medicine and Animal Sciences, Swedish University of Agricultural Sciences, 756 51 Uppsala, Sweden.

Search for other papers by Anne-Sofie Lagerstedt in
Current site
Google Scholar
PubMed
Close
 DVM, PhD
,
Ragnvi Hagman Department of Clinical Sciences, Faculty of Veterinary Medicine and Animal Sciences, Swedish University of Agricultural Sciences, 756 51 Uppsala, Sweden.

Search for other papers by Ragnvi Hagman in
Current site
Google Scholar
PubMed
Close
 DVM, PhD
,
Herman A. W. Hazewinkel Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, Utrecht University, 3508 TD Utrecht, The Netherlands.

Search for other papers by Herman A. W. Hazewinkel in
Current site
Google Scholar
PubMed
Close
 DVM, PhD
, and
Björn P. Meij Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, Utrecht University, 3508 TD Utrecht, The Netherlands.

Search for other papers by Björn P. Meij in
Current site
Google Scholar
PubMed
Close
 DVM, PhD

Abstract

Objective—To evaluate the reliability of the Thompson system for use in grading the gross pathological changes of intervertebral disk (IVD) degeneration in dogs and to investigate the agreement between gross pathological findings and low-field (0.2-T) magnetic resonance imaging (MRI) findings.

Sample—Vertebral columns from cadavers of 19 dogs of various ages, breeds, and origins.

Procedures—182 intervertebral segments were collected from 19 canine cadavers. Sagittal T2-weighted MRI of the T11 through S1 portion of the vertebral column was performed within 24 hours after the dogs were euthanized. The vertebral columns were subsequently divided in the midsagittal plane, and high-resolution photographs were obtained of each intervertebral segment (end plate—disk—end plate). The MRI images and photographs were graded separately in a blinded manner by 4 observers who used both Pfirrmann and Thompson grading criteria.

Results—The interobserver agreement for Thompson scores ranged from 0.76 to 0.88, and the intraobserver agreement ranged from 0.88 to 0.94 (Cohen weighted κ analysis). Agreement between scores for the Pfirrmann and Thompson grading criteria was κ = 0.70.

Conclusions and Clinical Relevance—Grading of IVD degeneration in dogs by use of the Thompson system resulted in high interobserver and intraobserver agreement, and scores for the Thompson system had substantial agreement with low-field MRI findings graded by use of the Pfirrmann system. This suggested that low-field MRI can be used to diagnose IVD degeneration in dogs.

Abstract

Objective—To evaluate the reliability of the Thompson system for use in grading the gross pathological changes of intervertebral disk (IVD) degeneration in dogs and to investigate the agreement between gross pathological findings and low-field (0.2-T) magnetic resonance imaging (MRI) findings.

Sample—Vertebral columns from cadavers of 19 dogs of various ages, breeds, and origins.

Procedures—182 intervertebral segments were collected from 19 canine cadavers. Sagittal T2-weighted MRI of the T11 through S1 portion of the vertebral column was performed within 24 hours after the dogs were euthanized. The vertebral columns were subsequently divided in the midsagittal plane, and high-resolution photographs were obtained of each intervertebral segment (end plate—disk—end plate). The MRI images and photographs were graded separately in a blinded manner by 4 observers who used both Pfirrmann and Thompson grading criteria.

Results—The interobserver agreement for Thompson scores ranged from 0.76 to 0.88, and the intraobserver agreement ranged from 0.88 to 0.94 (Cohen weighted κ analysis). Agreement between scores for the Pfirrmann and Thompson grading criteria was κ = 0.70.

Conclusions and Clinical Relevance—Grading of IVD degeneration in dogs by use of the Thompson system resulted in high interobserver and intraobserver agreement, and scores for the Thompson system had substantial agreement with low-field MRI findings graded by use of the Pfirrmann system. This suggested that low-field MRI can be used to diagnose IVD degeneration in dogs.

Intervertebral disk degeneration is common in dogs and humans and is often associated with severe problems in the lumbosacral region.1–4 Diseases related to IVD degeneration, such as disk herniation, degenerative lumbosacral stenosis, and cervical spondylomyelopathy, are common reasons for euthanasia in dogs. In humans, the lifetime prevalence for back problems is 60% to 80%, and 5% of affected individuals are subsequently unable to work.1,5 Diagnosis of IVD disease is made on the basis of physical and neurologic examination findings as well as information in the medical history and diagnostic imaging findings.6 Advanced imaging techniques, such as MRI and computed tomography, have been used in human medicine and are increasingly available in veterinary practice, where they have greatly facilitated the diagnosis of IVD disease in dogs.7 To detect and treat IVD disease earlier in the course of the condition, current diagnostic imaging techniques need to be refined. To achieve this, an accurate and reliable criterion-reference standard for macroscopic evaluation is needed.

It is important to distinguish between IVD degeneration and IVD disease. An IVD that gives rise to clinical signs as a result of disk herniation or instability of the vertebral column will invariably be degenerated; however, degenerated IVDs are also a common incidental finding in dogs without clinical signs of disease.3,8–10 In the study reported here, IVD degeneration was considered to include degeneration attributable to genetic or pathological reasons as well as to typical physiologic aging. It is difficult to distinguish between pathological and physiologic age-related changes in IVDs. Moreover, physiologically normal age-related changes (so-called senile remodeling) can ultimately lead to pathological conditions in IVDs.

Many similarities exist in IVD degeneration between humans and dogs. For example, the clinical signs, diagnostic methods and treatments used, loading patterns, and macroscopic and microscopic appearance are similar.11–14 However, although IVD degeneration is generally of the chondroid type in chondrodystrophic humans and dogs as well as achondroplastic humans, IVD degeneration is generally of the fibrous type in nonchondrodystrophic humans and dogs.8,13–18

In human medicine, there are established systems for scoring the severity of disk degeneration on the basis of histologic examination,19 radiography,20 MRI, and gross pathological changes. The most commonly used criterion-referenced standard for IVD degeneration in humans is the 5-category grading scheme for gross pathological changes developed by Thompson et al,21 although grading of disk degeneration on MRI in accordance with the system developed by Pfirrmann et al22 for evaluation of lumbar IVDs in humans is also used extensively23–25 Such scoring systems for IVD degeneration are not typically used in veterinary medicine. A grading system has been proposed for MRI images of lumbar IVDs by use of histologic examination as the criterion-referenced standard.26 In 1 study,27 investigators described MRI findings and the gross morphological appearance of degenerated canine IVDs, and investigators in another study7 reported the correlation between disk protrusion detected by use of MRI and computed tomography and surgical findings.28

To the authors' knowledge, the Thompson system has not been used to grade IVD degeneration in dogs, although there is no other scoring system available for evaluating the gross pathological changes of IVD degeneration in dogs. The purpose of the study reported here was to evaluate the reliability of the Thompson system for use in grading gross pathological changes of IVD degeneration in dogs and to investigate the agreement between gross pathological findings and low-field MRI findings.

Materials and Methods

Sample—The vertebral columns from 19 cadavers of dogs of various breeds and ages were included in the study. Dogs < 1 year old were not included because they rarely have disk degeneration.17 There were 5 Beagles, 2 Bouvier des Flandres, 3 Foxhounds, 3 Kerry Beagles, 1 Flat-Coated Retriever, 1 Welsh Terrier, and 4 mixed-breed dogs. The dogs (12 females and 7 males) ranged from 1 to 16 years of age and weighed 9 to 44 kg. The dogs were research dogs or client-owned dogs (with permission from the owners) that had been examined at the Utrecht University Clinic for Companion Animals. All dogs had been euthanized for reasons unrelated to the study reported here.

Collection and processing of the vertebral columns—The T11 through S1 vertebral segments were dissected from each of the 19 canine cadavers at a pathobiology laboratorya within 24 hours after the dogs were euthanized. Five of the vertebral segments were cut at T12 through L1 instead of at T11, which resulted in 182 intervertebral segments that were used in the study. The vertebral segments were wrapped in moist towels, and sagittal T2-weighted MRI images were obtained within 1 hour after segment dissection by use of a low-field (0.2-T) open magnetb with a 16-cm-diameter multipurpose flexible coil. It was necessary to dissect the vertebral segments before MRI because it was not possible to transport entire cadavers to the MRI facility. This might have led to a slight decrease in MRI resolution because the coil diameter was slightly larger than the diameter of the vertebral bodies, which can lead to a decrease in the signal-to-noise ratio. The MRI process included obtaining sagittal T2-weighted spin echo images (repetition time, 3,835 to 4,450 milliseconds; echo time, 117 milliseconds). The obtained MRI images had a slice thickness of 3 mm, and the slice that best depicted the IVD was selected for grading of IVD degeneration by use of the method of Pfirrmann et al.22

After MRI, the vertebrae were sectioned through the midline (sagittal plane) with a water-cooled belt saw, and the midsagittal cut surfaces of the intervertebral segments were cleaned to remove debris. Vertebrae were placed on a table. Multiple lights were used to illuminate the vertebrae from different directions, and high-resolution photographs were obtained by use of a digital single-lens reflex camerac equipped with a macro flash. A transparent ruler was placed on the cut surface as a scale marker. The digital photographs were cropped by use of photographic management softwared so that a single intervertebral segment was visible in each photograph. This was performed to prevent the observers who graded IVD degeneration from having knowledge about the source of the intervertebral segment (ie, location in the vertebral column) and also to prevent comparison with adjacent intervertebral segments. The photographs were used for the gross morphology grading of IVD degeneration in accordance with the method of Thompson et al.21

Pfirrmann grading of MRI images—The Pfirrmann system for grading IVD degeneration in human lumbar disks on midsagittal MRI images is a reliable method for use in grading IVDs of dogs.29 The grading system was based on 4 criteria (signal intensity, disk structure, disk height, and distinction between the nucleus and annulus; Appendix 1). The MRI images were converted to a digital format (ie, JPEG) and placed in a spreadsheet programe to prevent identification of the images by the observers; observers accessed the images via hyperlinks to the spreadsheet program. Grading was performed on T2-weighted MRI images; Pfirrmann scores ranged from grade 1 (healthy IVD) to 5 (end-stage IVD degeneration). Four observers (a veterinary medical student, a student in a PhD program, a board-certified veterinary surgeon, and a board-certified veterinary radiologist) separately graded the MRI images: none of the observers were aware of the source of the IVDs.

Thompson grading of photographs—The grading system described by Thompson et al21 is a 5-category method for assessing the gross morphology of mid-sagittal sections of human lumbar IVDs. Pathological changes of the nucleus pulposus, annulus fibrosus, end plates, and periphery of the vertebral body (Appendix 2) were graded by the same 4 observers who performed the Pfirrmann grading of MRI images, except that the board-certified radiologist was replaced by a board-certified veterinary pathologist. The photographs were provided to the observers in random order and in duplicate in a spreadsheet programe; they were accessed via hyperlinks to the spreadsheet program.

Statistical analysis—Interobserver and intraobserver reliability of the Thompson grading system were analyzed by use of Cohen weighted κ analysis, which calculated the percentage of agreement among the grades assigned to an image corrected by the chance that the same grade was assigned by chance. The weighted κ analysis provides more weight to grades that differ from each other by only 1 unit and less weight to grades that differ by > 1 unit. 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).30–32 To calculate interobserver reliability (the frequency of agreement between the 4 observers), grades assigned by the observer with the highest intraobserver agreement (the veterinary medical student, κ = 0.94) were selected for comparison with the grades assigned by the 3 other observers.

After evaluation of interobserver and intraobserver reliability, the mean of the values assigned by the 4 observers for all IVDs investigated (Pfirrmann grades for the MRI images and Thompson grades for the photographs) was calculated to enable analysis of the agreement between the Thompson grades and the degree of degeneration on MRI images. In cases in which there was a deviation of > 1 grade between the 4 observers, the image was reviewed again simultaneously by all 4 observers and a consensus decision was made. Agreement between the mean Pfirrmann and Thompson grades for each intervertebral segment was then analyzed by use of Cohen weighted κ analysis.

Results

Descriptive results—The frequency of IVD degeneration on the MRI images (Figure 1) and photographs (Figure 2) decreased in a similar pattern from grade 1 to 5. By use of the Pfirrmann scale, IVD degeneration in MRI images was assigned a grade of 1 for 71 of 182 (39.0%) intervertebral segments, a grade of 2 for 61 of 182 (33.5%) intervertebral segments, a grade of 3 for 41 of 182 (22.5%) intervertebral segments, a grade of 4 for 6 of 182 (3.3%) intervertebral segments, and a grade of 5 for 3 of 182 (1.6%) intervertebral segments. By use of the Thompson scale, IVD degeneration in photographs was assigned a grade of 1 for 61 of 182 (33.5%) intervertebral segments, a grade of 2 for 74 of 182 (40.7%) intervertebral segments, a grade of 3 for 27 of 182 (14.8%) intervertebral segments, a grade of 4 for 16 of 182 (8.8%) intervertebral segments, and a grade of 5 for 4 of 182 (2.2%) intervertebral segments.

Figure 1—
Figure 1—

A series of midsagittal T2-weighted MRI images of IVDs obtained from representative dogs. The images depict Pfirrmann grades from 1 (healthy IVD; far left) to 5 (end-stage IVD degeneration; far right).

Citation: American Journal of Veterinary Research 72, 7; 10.2460/ajvr.72.7.899

Figure 2—
Figure 2—

A series of photographs of IVDs obtained from representative dogs and divided in the midsagittal plane. The images depict Thompson grades from 1 (healthy IVD; far left) to 5 (end-stage IVD degeneration; far right).

Citation: American Journal of Veterinary Research 72, 7; 10.2460/ajvr.72.7.899

Intraobserver reliability of the Thompson system—Intraobserver reliability was almost perfect for all observers, with mean ± SE κ scores ranging from 0.94 ± 0.07 to 0.88 ± 0.07. In most cases (138/182 [75.8%] to 162/182 [89.0%]), the 2 photographs of the same intervertebral segment received the same grade. Differences between the grades for duplicate photographs were generally only 1 grade, although there was a difference of 2 grades for 2 intervertebral segments and a difference of 3 grades for 1 intervertebral segment.

Interobserver reliability of the Thompson system—Interobserver reliability was almost perfect (mean ± SE κ, 0.88 ± 0.07 to 0.83 ± 0.07) for 5 of 6 comparisons between observers and was substantial (mean ± SE κ, 0.76 ± 0.07) for 1 of 6 comparisons between observers.

Agreement between grades for the Pfirrmann system and Thompson system—Agreement was substantial (κ = 0.70) between mean grades for the Thompson system and mean grades for the Pfirrmann system. Agreement between grades for the Thompson and Pfirrmann systems was lower for the segments with IVD degeneration grades 4 and 5 than for the segments with IVD degeneration grades 1 to 3; however, there were fewer segments with severe (grades 4 and 5) IVD degeneration than with less severe (grades 1 to 3) IVD degeneration.

Discussion

Most diagnostic methods and treatments used in veterinary medicine have been adapted from methods and treatments used in human medicine. However, this is not always possible because of anatomic or physiologic differences between humans and other animal species. For this reason, new diagnostic methods, treatments, or surgical techniques need to be validated in the species in which they are intended for use before being implemented in veterinary practice. In the study reported here, we investigated whether the Thompson system used to grade IVD degeneration in humans could be applied to dogs. We found that the intraobserver and interobserver agreement for grading IVD degeneration by use of the Thompson system was almost perfect, which indicated that the Thompson system can be used to reliably grade IVD degeneration in cadavers of dogs.

To develop treatments for dogs with early IVD degeneration, diagnostic imaging methods with a high sensitivity and specificity for detecting early signs of disease are needed. This requires a reliable pathological-anatomic criterion-referenced standard that is reproducible and can be used to distinguish among stages of disease. The Thompson system fulfills these criteria and is the current criterion-referenced standard for research in IVD degeneration in humans.33–35 Thus, we chose the Thompson system for use in grading IVD degeneration in dogs. Other methods for determining the degree of disk degeneration include histologic examination and measurement of the glycosaminoglycan content of the nucleus.17,36–39 Although these methods have advantages, they lack the simplicity and overview of the Thompson system.

Although the Thompson grading system worked well when applied to IVDs of dogs, we detected inter-species differences in the development of vertebral lesions, with ventral and cranial spondylosis being common in dogs. In humans, spondylosis is generally associated with advanced stages of IVD degeneration,40 whereas spondylosis was encountered in only a few affected (and even some healthy) IVDs in the present study. This has been reported in the veterinary literature.26,41 The presence of spondylosis in vertebral segments with healthy or mildly degenerated IVDs might have biased the observers in assigning grades that were too high. According to the Thompson system, osteophytes should only be present in severe degeneration (grades 3 to 5), and osteophytes > 2 mm should only be present in the severest degeneration (grade 5). Thus, detection of spondylosis would be considered clinically relevant to IVD degeneration only when spondylosis is present in severely degenerated IVDs. Spondylosis in dogs is associated with type II disk herniation rather than with type I herniation,42 which supports the hypothesis that fibrous metaplasia of the IVD in dogs resembles IVD degeneration in humans.

By use of the Thompson system, there was an intraobserver difference of 2 grades for 2 intervertebral segments and of 3 grades in another intervertebral segment. We cannot explain these findings because these segments did not share features that distinguished them from the other intervertebral segments. Therefore, it is not clear whether there were clerical errors or whether the observer indeed perceived the degeneration as being markedly different between the 2 grading sessions.

Several factors could have influenced the Pfirrmann grading of IVD degeneration on MRI images of dogs. First, the dogs were of various ages, shapes, and sizes. Second, resolution of the disks is markedly lower in small-breed dogs than in large-breed dogs when low-field MRI is used because of the smaller size of the IVDs (image resolution is the same for small and large dogs).43,44 This could have led to inaccurate grading of the IVDs of small dogs. Third, T2-weighted MRI images were used because they best depict the glycosaminoglycan and water content of the disks, which in turn is correlated with the degree of disk degeneration. This means that the brighter the appearance of the nucleus on a T2-weighted MRI image, the higher the glycosaminoglycan content and the healthier the disk.22,36,37,40,45 The so-called coil effect of the MRI results in a brighter signal in the focus area of the magnetic field than in the adjacent areas of the vertebral column,46,47 which could lead to falsely low signals for the nucleus pulposus in IVDs located peripherally in the images and thus falsely high Pfirrmann scores. Moreover, the vertebral columns had been removed before MRI, which would have resulted in slightly decreased MRI resolution because the coil diameter was slightly larger than the diameter of the vertebral bodies, which would lead to a decreased signal-to-noise ratio.

The overall agreement between the mean grades for the Thompson system and the mean grades for the Pfirrmann system was substantial (κ, 0.70). Most IVDs with a Thompson grade of 1 or 2 were assigned a Pfirrmann grade of 1 or 2, and the deviation was ≤ 1 grade. However, for IVDs with a Thompson grade of 3, 4, or 5, the Pfirrmann grade deviated by up to 2 grades, and for IVDs with a Thompson grade of 4 or 5, less than half received the same Pfirrmann grades. Few disks graded by use of the Thompson and Pfirrmann systems had a grade of 4 (16 [8.8%] and 6 [3.3%], respectively) or 5 (4 [2.2%] and 3 [1.6%], respectively). These low frequencies may have contributed to the poor agreement between the systems for grades 4 and 5. Another factor that may have contributed to the low agreement is the intrinsic difference between the 2 grading systems. The Thompson system is based on changes in the nucleus, annulus, end plate, and vertebral body, whereas the Pfirrmann system is based on changes in the nucleus and annulus. Future studies should focus on the agreement between the MRI findings and the macroscopic appearance of high-grade IVD degeneration.

The high amount of agreement between macroscopic changes (graded by use of the Thompson system) and low-field MRI findings (graded by use of the Pfirrmann system) suggests that on the basis of the increasing availability of MRI in veterinary practices, MRI will become an increasingly useful tool for the diagnosis of IVD degeneration in dogs in a clinical setting. However, as previously stated, dogs often have degenerated IVDs without any clinical signs, so a finding of degenerated IVDs on MRI images will have to be substantiated by clinical and neurologic findings to reach an accurate diagnosis.

In the study reported here, we determined that the Thompson system was a reliable method for grading IVD degeneration in dogs, with a high interobserver and intraobserver agreement. Furthermore, there was substantial agreement between macroscopic grades of intervertebral segments assigned in accordance with the Thompson system and grades of low-field MRI images assigned in accordance with the Pfirrmann system, which suggests that evaluation of low-field MRI images can be used to diagnose IVD disease in dogs. The agreement was stronger in the earlier stages of degeneration (grades 1 to 3), which is advantageous because it enables early clinical intervention. However, because dogs may have subclinical IVD degeneration, it is important that clinical and neurologic findings be used to substantiate MRI findings of IVD degeneration to reach an accurate diagnosis.

ABBREVIATIONS

IVD

Intervertebral disk

MRI

Magnetic resonance imaging

a.

Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands.

b.

Magnetom Open Viva, Siemens AG, Munich, Germany.

c.

Nikon 10-megapixel digital SLR camera, Nikon, Tokyo, Japan.

d.

Microsoft Office picture manager, Microsoft Corp, Redmond, Wash.

e.

Microsoft Excel, professional edition 2003, Microsoft Corp, Redmond, Wash.

References

  • 1.

    Frymoyer JW, Cats-Baril WL. An overview of the incidences and costs of low back pain. Orthop Clin North Am 1991; 22: 263271.

  • 2.

    Maniadakis N, Gray A. The economic burden of back pain in the UK. Pain 2000; 84: 95103.

  • 3.

    Hoerlein BF. Intervertebral disc protrusions in the dog. I. Incidence and pathological lesions. Am J Vet Res 1953; 14: 260269.

  • 4.

    Gage ED. Incidence of clinical disc disease in the dog. J Am Anim Hosp Assoc 1975; 135: 135138.

  • 5.

    Freburger JK, Holmes GM, Agans RP, et al. The rising prevalence of chronic low back pain. Arch Intern Med 2009; 169: 251258.

  • 6.

    Fossum TW. Chapter 39, surgery of the thoracolumbar spine. Small animal surgery. 3rd ed. St Louis: Elsevier, 2007; 1470.

  • 7.

    Suwankong N, Voorhout G, Hazewinkel HA, et al. Agreement between computed tomography, magnetic resonance imaging, and surgical findings in dogs with degenerative lumbosacral stenosis. J Am Vet Med Assoc 2006; 229: 19241929.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8.

    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: 1117.

    • Search Google Scholar
    • Export Citation
  • 9.

    Jones JC, Inzana KD. Subclinical CT abnormalities in the lumbosacral spine of older large-breed dogs. Vet Radiol Ultrasound 2000; 41: 1926.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    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: 16011612.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Zimmerman MC, Vuono-Hawkins M, Parsons JR, et al. The mechanical properties of the canine lumbar disc and motion segment. Spine 1992; 17: 213220.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Bray JP, Burbidge HM. The canine intervertebral disk: part one: structure and function. J Am Anim Hosp Assoc 1998; 34: 5563.

  • 13.

    Lotz JC. Animal models of intervertebral disc degeneration: lessons learned. Spine 2004; 29: 27422750.

  • 14.

    Hansen HJ. A pathologic-anatomical interpretation of disc degeneration in dogs. Acta Orthop Scand 1951; 20: 280293.

  • 15.

    An HS, Masuda K. Relevance of in vitro and in vivo models for intervertebral disc degeneration. J Bone Joint Surg Am 2006; 88 (suppl 2): 8894.

    • Search Google Scholar
    • Export Citation
  • 16.

    Singh K, Masuda K, An HS. Animal models for human disc degeneration. Spine J 2005; 5: 267S279S.

  • 17.

    Bray JP, Burbidge HM. The canine intervertebral disk. Part two: degenerative changes—nonchondrodystrophoid versus chondrodystrophoid disks. J Am Anim Hosp Assoc 1998; 34: 135144.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Alini M, Eisenstein SM, Ito K, et al. Are animal models useful for studying human disc disorders/degeneration? Eur Spine J 2008; 17: 219.

  • 19.

    Boos N, Weissbach S, Rohrbach H, et al. Classification of age-related changes in lumbar intervertebral discs: 2002 Volvo Award in basic science. Spine 2002; 27: 26312644.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Lane NE, Nevitt MC, Genant HK, et al. Reliability of new indices of radiographic osteoarthritis of the hand and hip and lumbar disc degeneration. J Rheumatol 1993; 20: 19111918.

    • Search Google Scholar
    • Export Citation
  • 21.

    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: 411415.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Pfirrmann CW, Metzdorf A, Zanetti M, et al. Magnetic resonance classification of lumbar intervertebral disc degeneration. Spine 2001; 26: 18731878.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Griffith JF, Wang YX, Antonio GE, et al. Modified Pfirrmann grading system for lumbar intervertebral disc degeneration. Spine 2007; 32: E708E712.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Rajasekaran S, Venkatadass K, Naresh Babu J, et al. Pharmacological enhancement of disc diffusion and differentiation of healthy, ageing and degenerated discs: results from in-vivo serial post-contrast MRI studies in 365 human lumbar discs. Eur Spine J 2008; 17: 626643.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Scuderi GJ, Brusovanik GV, Golish SR, et al. A critical evaluation of discography in patients with lumbar intervertebral disc disease. Spine J 2008; 8: 624629.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    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: 179184.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Sether LA, Nguyen C, Yu SN, et al. Canine intervertebral disks: correlation of anatomy and MR imaging. Radiology 1990; 175: 207211.

  • 28.

    Coates JR. Intervertebral disk disease. Vet Clin North Am Small Anim Pract 2000; 30: 77110.

  • 29.

    Bergknut N, Auriemma E, Wijsman S, et al. Evaluation of intervertebral disk degeneration in chondrodystrophic and nonchondrodystrophic dogs by use of Pfirrmann grading of images obtained with low-field magnetic resonance imaging. Am J Vet Res 2011; 72: 899904.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977; 33: 159174.

  • 31.

    Landis JR, Koch GG. An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics 1977; 33: 363374.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    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: 133158.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Singh K, Masuda K, Thonar EJ, et al. Age-related changes in the extracellular matrix of nucleus pulposus and anulus fibrosus of human intervertebral disc. Spine 2009; 34: 1016.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Patel KP, Sandy JD, Akeda K, et al. Aggrecanases and aggrecanasegenerated fragments in the human intervertebral disc at early and advanced stages of disc degeneration. Spine 2007; 32: 25962603.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Rutges J, Kummer J, Oner F, et al. Increased MMP-2 activity during intervertebral disc degeneration is correlated to MMP-14 levels. J Pathol 2008; 214: 523530.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Ghosh P, Taylor TK, Braund KG. Variation of the glycosaminoglycans of the intervertebral disc with ageing. II. Non-chondrodystrophoid breed. Gerontology 1977; 23: 99109.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Ghosh P, Taylor TK, Braund KG. The variation of the glycosaminoglycans of the canine intervertebral disc with ageing. I. Chondrodystrophoid breed. Gerontology 1977; 23: 8798.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Nguyen AM, Johannessen W, Yoder JH, et al. Noninvasive quantification of human nucleus pulposus pressure with use of T1rho-weighted magnetic resonance imaging. J Bone Joint Surg Am 2008; 90: 796802.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    Gruber HE, Ingram J, Hanley EN Jr. An improved staining method for intervertebral disc tissue. Biotech Histochem 2002; 77: 8183.

  • 40.

    Adams MA, Roughley PJ. What is intervertebral disc degeneration, and what causes it? Spine 2006; 31: 21512161.

  • 41.

    Wright JA. Spondylosis deformans of the lumbo-sacral joint in dogs. J Small Anim Pract 1980; 21: 4558.

  • 42.

    Levine GJ, Levine JM, Walker MA, et al. Evaluation of the association between spondylosis deformans and clinical signs of intervertebral disk disease in dogs: 172 cases (1999–2000). J Am Vet Med Assoc 2006; 228: 96100.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43.

    Cihangiroglu M, Yildirim H, Bozgeyik Z, et al. Observer variability based on the strength of MR scanners in the assessment of lumbar degenerative disc disease. Eur J Radiol 2004; 51: 202208.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44.

    Nijeholt GJ, Bergers E, Kamphorst W, et al. Post-mortem high-resolution MRI of the spinal cord in multiple sclerosis: a correlative study with conventional MRI, histopathology and clinical phenotype. Brain 2001; 124: 154166.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    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: 4243.

    • Search Google Scholar
    • Export Citation
  • 46.

    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: 891898.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47.

    Seeger LL. Physical principles of magnetic resonance imaging. Clin Orthop Relat Res 1989; 244: 716.

Appendix 1

Description of the MRI-based grading system used to classify IVDs in dogs.

Pfirrmann gradeStructureDistinction between NP and AFSignal intensityHeight of IVD
   1Homogeneous and brightwhiteClearHyperintense and isointenseto CSFNormal
   2Nonhomogeneous with or without horizontal bandsClearHyperintense and isointenseto CSFNormal
   3Nonhomogeneous and grayUnclearIntermediateNormal to slightly decreased
   4Nonhomogeneous and gray to blackLostIntermediate to hypointenseNormal to moderately decreased
   5Nonhomogeneous and blackLostHypointenseCollapsed 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.)

Appendix 2

Description of the macroscopic grading scheme used to classify gross pathological changes of IVDs in dogs.

Thompson gradeNucleus pulposusAnnulus fibrosusEnd platesVertebral bodies
   1Bulging gelDiscrete fibrous lamellaeHyaline; uniform thicknessRounded margins
   2White fibrous tissue peripherallyMucinous material between lamellaeIrregular thicknessPointed margins
   3Consolidated fibrous tissueExtensive mucinous infiltration; loss of annular-nuclear demarcationFocal defects in cartilageEarly chondrophytes or osteophytes at margins
   4Horizontal (vertical) clefts parallel to end plateFocal disruptionsFibrocartilage extending from subchondral bone; irregularity and focal sclerosis in subchondral boneOsteophytes < 2 mm
   5Clefts extend through nucleus and annulus Diffuse sclerosisOsteophytes > 2 mm

(Adapted from 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. Reprinted with permission.)

  • Figure 1—

    A series of midsagittal T2-weighted MRI images of IVDs obtained from representative dogs. The images depict Pfirrmann grades from 1 (healthy IVD; far left) to 5 (end-stage IVD degeneration; far right).

  • Figure 2—

    A series of photographs of IVDs obtained from representative dogs and divided in the midsagittal plane. The images depict Thompson grades from 1 (healthy IVD; far left) to 5 (end-stage IVD degeneration; far right).

  • 1.

    Frymoyer JW, Cats-Baril WL. An overview of the incidences and costs of low back pain. Orthop Clin North Am 1991; 22: 263271.

  • 2.

    Maniadakis N, Gray A. The economic burden of back pain in the UK. Pain 2000; 84: 95103.

  • 3.

    Hoerlein BF. Intervertebral disc protrusions in the dog. I. Incidence and pathological lesions. Am J Vet Res 1953; 14: 260269.

  • 4.

    Gage ED. Incidence of clinical disc disease in the dog. J Am Anim Hosp Assoc 1975; 135: 135138.

  • 5.

    Freburger JK, Holmes GM, Agans RP, et al. The rising prevalence of chronic low back pain. Arch Intern Med 2009; 169: 251258.

  • 6.

    Fossum TW. Chapter 39, surgery of the thoracolumbar spine. Small animal surgery. 3rd ed. St Louis: Elsevier, 2007; 1470.

  • 7.

    Suwankong N, Voorhout G, Hazewinkel HA, et al. Agreement between computed tomography, magnetic resonance imaging, and surgical findings in dogs with degenerative lumbosacral stenosis. J Am Vet Med Assoc 2006; 229: 19241929.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8.

    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: 1117.

    • Search Google Scholar
    • Export Citation
  • 9.

    Jones JC, Inzana KD. Subclinical CT abnormalities in the lumbosacral spine of older large-breed dogs. Vet Radiol Ultrasound 2000; 41: 1926.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    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: 16011612.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Zimmerman MC, Vuono-Hawkins M, Parsons JR, et al. The mechanical properties of the canine lumbar disc and motion segment. Spine 1992; 17: 213220.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Bray JP, Burbidge HM. The canine intervertebral disk: part one: structure and function. J Am Anim Hosp Assoc 1998; 34: 5563.

  • 13.

    Lotz JC. Animal models of intervertebral disc degeneration: lessons learned. Spine 2004; 29: 27422750.

  • 14.

    Hansen HJ. A pathologic-anatomical interpretation of disc degeneration in dogs. Acta Orthop Scand 1951; 20: 280293.

  • 15.

    An HS, Masuda K. Relevance of in vitro and in vivo models for intervertebral disc degeneration. J Bone Joint Surg Am 2006; 88 (suppl 2): 8894.

    • Search Google Scholar
    • Export Citation
  • 16.

    Singh K, Masuda K, An HS. Animal models for human disc degeneration. Spine J 2005; 5: 267S279S.

  • 17.

    Bray JP, Burbidge HM. The canine intervertebral disk. Part two: degenerative changes—nonchondrodystrophoid versus chondrodystrophoid disks. J Am Anim Hosp Assoc 1998; 34: 135144.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Alini M, Eisenstein SM, Ito K, et al. Are animal models useful for studying human disc disorders/degeneration? Eur Spine J 2008; 17: 219.

  • 19.

    Boos N, Weissbach S, Rohrbach H, et al. Classification of age-related changes in lumbar intervertebral discs: 2002 Volvo Award in basic science. Spine 2002; 27: 26312644.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Lane NE, Nevitt MC, Genant HK, et al. Reliability of new indices of radiographic osteoarthritis of the hand and hip and lumbar disc degeneration. J Rheumatol 1993; 20: 19111918.

    • Search Google Scholar
    • Export Citation
  • 21.

    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: 411415.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Pfirrmann CW, Metzdorf A, Zanetti M, et al. Magnetic resonance classification of lumbar intervertebral disc degeneration. Spine 2001; 26: 18731878.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Griffith JF, Wang YX, Antonio GE, et al. Modified Pfirrmann grading system for lumbar intervertebral disc degeneration. Spine 2007; 32: E708E712.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Rajasekaran S, Venkatadass K, Naresh Babu J, et al. Pharmacological enhancement of disc diffusion and differentiation of healthy, ageing and degenerated discs: results from in-vivo serial post-contrast MRI studies in 365 human lumbar discs. Eur Spine J 2008; 17: 626643.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Scuderi GJ, Brusovanik GV, Golish SR, et al. A critical evaluation of discography in patients with lumbar intervertebral disc disease. Spine J 2008; 8: 624629.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    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: 179184.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Sether LA, Nguyen C, Yu SN, et al. Canine intervertebral disks: correlation of anatomy and MR imaging. Radiology 1990; 175: 207211.

  • 28.

    Coates JR. Intervertebral disk disease. Vet Clin North Am Small Anim Pract 2000; 30: 77110.

  • 29.

    Bergknut N, Auriemma E, Wijsman S, et al. Evaluation of intervertebral disk degeneration in chondrodystrophic and nonchondrodystrophic dogs by use of Pfirrmann grading of images obtained with low-field magnetic resonance imaging. Am J Vet Res 2011; 72: 899904.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977; 33: 159174.

  • 31.

    Landis JR, Koch GG. An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics 1977; 33: 363374.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    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: 133158.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Singh K, Masuda K, Thonar EJ, et al. Age-related changes in the extracellular matrix of nucleus pulposus and anulus fibrosus of human intervertebral disc. Spine 2009; 34: 1016.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Patel KP, Sandy JD, Akeda K, et al. Aggrecanases and aggrecanasegenerated fragments in the human intervertebral disc at early and advanced stages of disc degeneration. Spine 2007; 32: 25962603.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Rutges J, Kummer J, Oner F, et al. Increased MMP-2 activity during intervertebral disc degeneration is correlated to MMP-14 levels. J Pathol 2008; 214: 523530.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Ghosh P, Taylor TK, Braund KG. Variation of the glycosaminoglycans of the intervertebral disc with ageing. II. Non-chondrodystrophoid breed. Gerontology 1977; 23: 99109.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Ghosh P, Taylor TK, Braund KG. The variation of the glycosaminoglycans of the canine intervertebral disc with ageing. I. Chondrodystrophoid breed. Gerontology 1977; 23: 8798.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Nguyen AM, Johannessen W, Yoder JH, et al. Noninvasive quantification of human nucleus pulposus pressure with use of T1rho-weighted magnetic resonance imaging. J Bone Joint Surg Am 2008; 90: 796802.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    Gruber HE, Ingram J, Hanley EN Jr. An improved staining method for intervertebral disc tissue. Biotech Histochem 2002; 77: 8183.

  • 40.

    Adams MA, Roughley PJ. What is intervertebral disc degeneration, and what causes it? Spine 2006; 31: 21512161.

  • 41.

    Wright JA. Spondylosis deformans of the lumbo-sacral joint in dogs. J Small Anim Pract 1980; 21: 4558.

  • 42.

    Levine GJ, Levine JM, Walker MA, et al. Evaluation of the association between spondylosis deformans and clinical signs of intervertebral disk disease in dogs: 172 cases (1999–2000). J Am Vet Med Assoc 2006; 228: 96100.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43.

    Cihangiroglu M, Yildirim H, Bozgeyik Z, et al. Observer variability based on the strength of MR scanners in the assessment of lumbar degenerative disc disease. Eur J Radiol 2004; 51: 202208.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44.

    Nijeholt GJ, Bergers E, Kamphorst W, et al. Post-mortem high-resolution MRI of the spinal cord in multiple sclerosis: a correlative study with conventional MRI, histopathology and clinical phenotype. Brain 2001; 124: 154166.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    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: 4243.

    • Search Google Scholar
    • Export Citation
  • 46.

    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: 891898.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47.

    Seeger LL. Physical principles of magnetic resonance imaging. Clin Orthop Relat Res 1989; 244: 716.

Advertisement