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Treatment recommendations differ for dogs with intervertebral disk extrusion vs. intervertebral disk protrusion.
The aim of this retrospective, cross-sectional study was to determine whether clinical and magnetic resonance
imaging (MRI) variables could be used to predict a diagnosis of thoracolumbar intervertebral disk extrusion or
protrusion in dogs. Dogs were included if they were large breed dogs, had an MRI study of the thoracolumbar
or lumbar vertebral column, had undergone spinal surgery, and had the type of intervertebral disk hernia-
tion (intervertebral disk extrusion or protrusion) clearly stated in surgical reports. A veterinary neurologist
unaware of surgical findings reviewed MRI studies and recorded number, location, degree of degeneration
and morphology of intervertebral disks, presence of nuclear clefts, disk space narrowing, extent, localization
and lateralization of herniated disk material, degree of spinal cord compression, intraparenchymal intensity
changes, spondylosis deformans, spinal cord swelling, spinal cord atrophy, vertebral endplate changes, and
presence of extradural hemorrhage. Ninety-five dogs were included in the sample. Multivariable statistical
models indicated that longer duration of clinical signs (P = 0.01), midline instead of lateralized disk herniation
(P = 0.007), and partial instead of complete disk degeneration (P = 0.01) were associated with a diagnosis
of intervertebral disk protrusion. The presence of a single intervertebral herniation (P = 0.023) and dispersed
intervertebral disk material not confined to the disk space (P = 0.06) made a diagnosis of intervertebral
disk extrusion more likely. Findings from this study identified one clinical and four MRI variables that could
potentially facilitate differentiating intervertebral disk extrusions from protrusions in dogs.
C 2016 American
Key words: disk herniation, disk prolapse, intervertebral disk, intervertebral disk disease.
1
2 GOMES ET AL. 2016
extrusions and protrusions are also associated with differ- tebral disk disease, and MRI. Dogs were included if
ent suggested treatment options,4,10,1214 and possibly also a (1) they were large breed dogs, defined as a body weight
different prognosis.4 Intervertebral disk extrusions are typ- exceeding 20 kg,4 (2) underwent an MRI study of the tho-
ically treated by a hemilaminectomy.5 Several studies have, racolumbar or lumbar vertebral column, (3) following a di-
however, suggested this type of surgery would be inadequate agnosis of intervertebral disk herniation underwent spinal
for intervertebral disk protrusions and have suggested alter- surgery consisting of a hemilaminectomy or hemilaminec-
native surgical approaches, including additional vertebral tomy combined with a partial discectomy, and (4) the type
stabilization10 or a lateral corpectomy.12,13 While a hemil- of intervertebral disk herniation (intervertebral disk extru-
aminectomy is considered a basic spinal surgical technique, sion or protrusion) was clearly noted in the surgical reports.
and vertebral stabilization and lateral corpectomy should Dogs were excluded if the medical records or imaging stud-
be considered more technically demanding. Treatment of ies were incomplete, if they were not available in a digi-
intervertebral disk protrusions is further complicated by the tal format, or if the type of intervertebral disk herniation
fact that little is known about the results of medical man- (extrusion or protrusion) was not clearly noted in the surgi-
agement and that dogs with protrusions are at increased risk cal reports. Dogs were also excluded if more than one type
of early postoperative neurological deterioration compared of intervertebral disk herniation (both intervertebral disk
to dogs with extrusions.4 It seems, therefore, important to extrusion and protrusion), or acute herniations of flaps of
accurately differentiate thoracolumbar intervertebral disk anulus were observed during surgery. For inclusion in the
extrusions from protrusions before treatment options and study, the surgical treatment had to have consisted of a de-
associated outcomes are discussed with owners of affected compressive hemilaminectomy, a hemilaminectomy com-
dogs. Currently, the exact type of intervertebral disk hernia- bined with an anulectomy, or a hemilaminectomy combined
tion can only be recognized during surgery. If we want to im- with a partial discectomy. During the latter procedure, a
prove our knowledge on the natural evolution and results of hemilaminectomy had to have been initially performed to
different treatment modalities, including medical manage- allow inspection of the vertebral canal. This had to have
ment, we should improve our knowledge on how to differ- been followed by a lateral approach to the affected inter-
entiate both types of intervertebral disk herniation without vertebral disk, after which the dorsal part of the disk and
surgical confirmation. Although intervertebral disk herni- a portion of the adjacent vertebral endplates were removed
ation can be diagnosed by a variety of imaging modalities, by a pneumatic drill or surgical aspirator. For inclusion, all
MRI is considered the imaging modality of choice.15 Sev- dogs had to have undergone MRI under general anesthe-
eral studies have reported MRI findings in dogs with thora- sia (1.5T, Intera, Philips Medical Systems, Eindhoven, the
columbar intervertebral disk herniations,1620 establishing Netherlands). If dogs had MRI on multiple occasions for
further insights into the pathophysiology, grading, diagno- confirmed intervertebral disk herniation, only information
sis, treatment, and prognosis of this disorder. No studies from the first visit was used.
have, however, evaluated if specific clinical or MRI abnor-
malities can be used to differentiate between thoracolum-
Data Recorded
bar intervertebral disk extrusions and protrusions. The aim
of this retrospective, cross-sectional study was therefore to Information retrieved from the medical records included
determine whether clinical and previously reported MRI signalment, duration, type, and severity of clinical signs,
characteristics could be used to differentiate between these general physical and neurological examinations findings,
two specific types of intervertebral disk herniation. It was and type of surgery. Severity of neurological deficits was
hypothesized that specific clinical and MRI variables exist graded by the modified Frankel score,21 which was defined
that could independently predict the occurrence of inter- as paraplegia with no deep nociception (grade 0), para-
vertebral disk extrusion or protrusion. plegia with no superficial nociception (grade 1), paraple-
gia with nociception (grade 2), nonambulatory paraparesis
(grade 3), ambulatory paraparesis and ataxia (grade 4),
Materials and Methods spinal hyperesthesia only (grade 5), or no dysfunction.
Magnetic resonance imaging studies were anonymized
Criteria for Animal Selection
and presented in a randomized order to a board-certified
The digital medical database of the Royal Veterinary Col- veterinary neurologist (S.D.D.). The observer was only in-
lege was searched between July 2002 and January 2014 for formed of the location of the surgically confirmed inter-
large breed dogs that had undergone MRI and decompres- vertebral disk herniation or herniations and only T1- and
sive surgery for thoracolumbar or lumbar intervertebral T2-weighted sequences were presented and assessed. Stan-
disk herniation. Search terms were intervertebral disk ex- dard image archiving and communication system software
trusion, intervertebral disk protrusion, intervertebral (Osirix Foundation, V.5.5.2 Geneva, Switzerland) was used
disk herniation, intervertebral disk prolapse, interver- to view and assess the imaging studies. The selection of
VOL. 00, NO. 0 MRI OF THORACOLUMBAR INTERVERTEBRAL DISK DISEASE 3
MRI variables was based on earlier reported veterinary ated with a decrease in nucleus pulposus signal intensity
studies5,16,2233 and covered several aspects of intervertebral on T2-weighted images,23 assessment of intervertebral disk
disk disease (Table 1). Assessed variables included number, degeneration was based on nucleus pulposus signal inten-
degree of degeneration and morphology of affected inter- sity on midsagittal T2-weighted images. A nondegenerate
vertebral disks, presence of nuclear clefts, narrowing of the disk (grade 0) had a homogenous hyperintense signal, a
intervertebral disk space, extent, localization and lateral- partially degenerate disk (grade 1) had heterogeneous loss
ization of herniated disk material, degree of spinal cord of hyperintense signal, and a completely degenerate inter-
compression, occurrence and type of intraparenchymal in- vertebral disk (grade 2) had complete loss of hyperintense
tensity changes, occurrence of spondylosis deformans ven- signal.26 Intervertebral disk morphology was described as
tral to the affected intervertebral disk space, spinal cord bulging, protrusion, or extrusion (Fig. 1).16 Bulging was
swelling, spinal cord atrophy, occurrence and type of ver- defined as a symmetric, uniform, and circumferential ex-
tebral endplate changes, and presence of extradural hem- tension of the disk margin over the border of the verte-
orrhage. Since intervertebral disk degeneration is associ- bral endplate; protrusion was defined as a focal midline or
TABLE 1. Results of Univariate Statistical Analysis for Clinical and MRI Variables for 52 Dogs with Intervertebral Disk Extrusion and 43 Dogs with
Intervertebral Disk Protrusion
FIG. 1. T2W transverse images of dogs with a surgically confirmed thoracolumbar intervertebral disk protrusion (A and B) and a dog with surgically
confirmed intervertebral disk extrusion (C). (A and B) Midline intervertebral disk herniation (arrows) was predictive for a diagnosis of disk protrusion,
while lateralized intervertebral disk herniation (arrow) was predictive for intervertebral disk extrusion (C). Presented intervertebral disk herniations represent
protrusion (A), bulging (B), and extrusion (C) morphology.
dorsolateral extension of the disk margin with focal rup- presence of spinal cord atrophy was defined as a subjectively
ture of the anulus fibrosus; extrusion was defined as pres- increased area of cerebrospinal fluid and epidural fat rela-
ence of herniated disk material through all layers of the tive to a decreased spinal cord area.24 Degree of spinal cord
anulus fibrosus.16 Intervertebral disk morphology was fur- compression was determined by calculating the remaining
ther determined by the ability or inability to observe the spinal cord area and compression ratio at the site of max-
well-defined contour of the anulus fibrosus on transverse imum spinal cord compression. The remaining spinal cord
T1-weighted images25 and the ability or inability to iden- area was defined as the cross-sectional area of the spinal
tify the distinction between the anulus fibrosus and nucleus cord of the compressed area divided by the cross-sectional
pulposus on midsagittal T2-weighted images.30 Narrowing area at the adjacent, noncompressed segment.22,33 The
of the intervertebral disk space was assessed subjectively by compression ratio was determined by dividing the smallest
visually comparing the affected intervertebral disk space dorsoventral diameter of the spinal cord by the broadest
maximum width with the adjacent, cranial, and caudal, transverse diameter at the same level.22,33 Intraparenchy-
nonaffected intervertebral disk spaces.31 Nuclear clefts were mal signal intensity changes were assessed on sagittal im-
defined as a focal area of signal loss in the nucleus pulposus ages and classified as: absent intraparenchymal signal inten-
on T2-weighted images.25 Localization of herniated disk sity changes on T2- or T1-weighted images (grade 0); light
material was assessed on T1- and T2-weighted transverse (obscure) hyperintense intraparenchymal signal intensity
images, being defined as ventral, lateral, or dorsal relative change on T2-weighted images (grade 1); intense (bright)
to the spinal cord. Lateralization of herniated material was hyperintense intraparenchymal signal intensity change on
further described as being exclusively in the midline or later- T2-weighted images (grade 2); hyperintense intraparenchy-
alized. Lateralized intervertebral disk herniations included mal signal intensity change on T2-weighted images, which
herniations in which the material was located ventrolateral, corresponded to a hypointense intraparenchymal signal in-
lateral, or dorsolateral on transverse images. Extension of tensity change on T1-weighted images (grade 3).32 Vertebral
herniated disk material was assessed on T2-weighted sagit- endplate changes were classified as: no changes (grade 0);
tal images and characterized as dispersed or confined to hypointense areas on T1-weighted images and hyperintense
the intervertebral disk space. Dispersed disk material was areas on T2-weighted images (grade 1); hyperintense areas
defined as herniated disk material with no clear association on T1-weighted images and areas of isointense or slightly
with its original intervertebral disk space.5,16 Disk material hyperintense signal intensity on T2-weighted images
confined to the intervertebral disk space was defined as her- (grade 2); hypointense signal on both T1- and T2-weighted
niated disk material, which did not exceed the limits of the images (grade 3).16 Presence of extradural hemorrhage was
disk space or associated vertebral endplates.12,29 Presence defined as a poorly demarcated, extradural area of hetero-
of spinal cord swelling and spinal cord atrophy were sub- geneous intensity on T2-weighted images.28
jectively evaluated on T2-weighted sagittal and transverse
images at the spinal segments immediately adjacent to the
Statistical Analyses
site of spinal cord compression. Spinal cord swelling was de-
fined as a subjectively decreased area of cerebrospinal fluid Statistical analysis was performed by one of the au-
and fat relative to a increased area of spinal cord, while the thors (R.M.A.P.) and data were analyzed using statistical
VOL. 00, NO. 0 MRI OF THORACOLUMBAR INTERVERTEBRAL DISK DISEASE 5
software (IBM SPSS Statistics version 19, NY). The bi- 0.3 mm in both planes. The transverse images were aligned
nomial outcome variable was diagnosis of intervertebral parallel to the respective intervertebral disks and for all
disk extrusion or protrusion. Associations between the 32 dogs, the area between the third thoracic vertebra and
predictor variables (clinical and MRI characteristics) and sacrum was included in the sagittal plane. The surgical
the outcome variable were screened at the univariable level appearance of intervertebral disk extrusions was typically
using Chi-squared analysis for categorical predictors, and characterized as sequestered calcified intervertebral disk
the Students t-test or MannWhitney U test for continuous material without physical connection with the ruptured
variables, dependent upon the normality of the distribution anulus fibrosus. The surgical appearance of interverte-
of the data, which was determined via visual inspection of bral disk protrusion was typically characterized by a focal
histograms. P values <0.05 were considered significant in or broad-based dorsal displacement of the intervertebral
all analyses. Variables significantly associated with diagno- disk without any defect in the outer layers of the anulus
sis at the univariable level (P < 0.05) were taken forward fibrosus.
to be tested in a multivariable model; a binomial logistic Breed distribution of 52 dogs with intervertebral disk
regression with diagnosis as the binomial outcome variable, extrusion was German Shepherd Dog (n = 12), Cross-
using intervertebral disc extrusion as the reference category. breed (seven), Labrador Retriever (six), Basset Hound,
Odds ratios of significant variables were inspected to deter- English Staffordshire Bull Terrier (both five), Clumber
mine which type of disc disease was more likely based on Spaniel, Rottweiler (both four), Rough Collie, Doberman
the predictor variables. Multicollinearity was checked for Pinscher, English Pointer, Golden Retriever, Lurcher, En-
in all models, identified from inflated standard errors in glish Bull Terrier, Portuguese Waterdog, English Springer
the models and thus avoided. Model fit was assessed using Spaniel, and Weimaraner (one for each). This group in-
the Akaikes information criterion (AIC) and percentage cluded 27 males and 25 females aged between 1 and
correct classification, with lower AIC models favored to re- 12 years (mean, 6.7 years). Median duration of clinical
duce residual error in the model while avoiding overfitting. signs, before referral, was 2 days (25th75th percentile,
In addition to these analyses, a post hoc receiver operat- 19.25 days). Dogs presented with neurological grades
ing characteristic (ROC) analysis was used to examine the 0 (n = 4 dogs), 1 (1), 2 (13), 3 (15), and 4 (19). Affected
performance of the significant continuous variable in the intervertebral disk spaces in order of occurrence were T13-
final model, duration of clinical signs, as an indicator of di- L1, L1-L2 (both n = 11), T12-T13 (nine), L3-L4 (seven),
agnosis by determining the diagnostic power of the test by L2-L3 (six), T11-T12, L4-L5 (both three), T3-T4 and
measuring the area under the curve (AUC). The reference T10-L1 (both one). All dogs underwent a decompressive
standard was surgically confirmed diagnosis of interverte- hemilaminectomy.
bral disk extrusion or protrusion. A perfect test has an AUC Breed distribution of 43 dogs with intervertebral disk
value of 1.0, with an AUC of 0.5 means the test performs protrusion was German Shepherd Dog (n = 21), English
no better than chance. Youdens index (Youdens J statistic; Staffordshire Bull Terrier (eight), Cross-breed (four), Bas-
J = Sensitivity + specificity 1) was calculated to identify set Hound (three), Labrador Retriever (two), Bullmas-
the optimal cutoff value of duration of clinical signs that tiff, Dalmatian, English Pointer, Golden Retriever and
yielded maximum sums from the ROC curves.
TABLE 2. Results of Multivariate Statistical Analysis for Clinical and
MRI Variables for 52 Dogs with Intervertebral Disk Extrusion and 43
Results Dogs with Intervertebral Disk Protrusion
FIG. 3. T2W sagittal images of a clinically normal dog (A), a dog with surgically confirmed thoracolumbar intervertebral disk protrusion (B), and a dog with
a surgically confirmed intervertebral disk extrusion (C). Partial loss of nucleus pulposus signal intensity (B) was associated with disk protrusion, while complete
loss of hyperintense signal (C) was associated with disk extrusion. Nondegenerated disk with homogenous hyperintense nucleus pulposus for comparison (A).
VOL. 00, NO. 0 MRI OF THORACOLUMBAR INTERVERTEBRAL DISK DISEASE 7
FIG. 4. T2W sagittal images of a dog with surgically confirmed thoracolumbar intervertebral disk protrusions (A), and a dog with intervertebral disk
extrusion (B). (A) Presence of multiple intervertebral disk herniations was predictive for a diagnosis of disk protrusion (arrows), while presence of a single
intervertebral disk herniation (arrow) was predictive for disk extrusion (B).
FIG. 5. T2W sagittal images of a dog with two surgically confirmed thoracolumbar intervertebral disk protrusions (A), and a dog with a surgically confirmed
intervertebral disk extrusion (B). Presence of herniated disk material confined to the intervertebral disk space (arrows) was predictive for protrusion (A), while
herniated disk material exceeding the limits of the intervertebral disk space (arrows) was predictive for extrusion (B). Both intervertebral disk protrusions (A)
demonstrate partial intervertebral disk degeneration, while the intervertebral disk extrusion (B) demonstrates complete intervertebral disk degeneration.
atrophy, lower compression ratio values (indicating more of complete intervertebral disk degeneration (Fig. 3) were
pronounced dorsoventral spinal cord flattening), presence significantly associated with a diagnosis of intervertebral
and type of intraparenchymal signal intensity changes, pres- disk protrusion. The presence of a single instead of mul-
ence and type of endplate changes, presence of multiple in- tiple intervertebral disk herniations (Fig. 4) and dispersed
tervertebral disk herniations, and presence of spondylosis intervertebral disk material not confined to the disk space
deformans were significantly associated with a diagnosis (Fig. 5) made a diagnosis of intervertebral disk extrusion
of intervertebral disk protrusion. After performing bino- more likely. Although the latter variable did not reach sta-
mial logistic regression, four MRI variables were retained tistical significance (P = 0.06), inclusion of this variable
as independent predictors of intervertebral disk protrusion improved model fit (determined by AIC values and per-
or extrusion (Table 2). Midline instead of lateralized in- centage correct classification) and it was thus retained in
tervertebral disk herniation (Fig. 1), and partial instead the final model.
8 GOMES ET AL. 2016
have contributed to the higher number of disk herniations that this study did not evaluate the diagnostic accuracy or
in dogs with intervertebral disk protrusions. Occurrence reliability of the blinded observer and that interpretation of
of multiple lumbar disk protrusions poses difficulties in most evaluated MRI variables were likely associated with
selecting the most appropriate treatment modality. While inherent subjectivity. Previous studies have questioned the
specific surgical techniques, including stabilization, have reliability of some of the evaluated MRI variables, includ-
been suggested10,13 , the presence of multiple disk protru- ing subjective evaluation of intervertebral disk width.41,42
sions has also been associated with a reluctance to perform Subjective evaluation of intervertebral disk width using
surgery.4 MRI has been associated with considerable disagreement
In agreement with previous findings,4 dispersion of her- between and within observers,41,42 while objective measure-
niated disk material beyond the borders of the affected ments have been associated with good inter- and intraob-
disk space was associated with a diagnosis of intervertebral server agreement.43 Absolute measurements were however
disk extrusion, while confinement to the borders of the in- not included in this study due to concerns about hetero-
tervertebral disk space was associated with a diagnosis of geneity of included breeds and dog sizes. Although this
intervertebral disk protrusion. This finding can most likely study has identified one clinical and four MRI variables
be explained by the fact that the dorsally displaced nucleus that are independently associated with a diagnosis of inter-
pulposus remains contained within the outer layers of the vertebral disk extrusion or protrusion, it is currently unclear
anulus fibrosus in dogs with disk protrusions,3,6,9 while cal- if application of these variables into a clinical setting will
cified nucleus pulpous ruptures through all layers of the consistently result in an improved differentiating of both
anulus in dogs with intervertebral disk extrusion and can clinical entities. Furthermore, it is currently unclear how
therefore be more easily displaced beyond the boundaries well or poor intervertebral disk extrusion and protrusion
of the affected intervertebral disk space.5 can be differentiated without assistance of these variables.
This study is limited by its retrospective nature, which Further studies are therefore needed to determine the ne-
complicated standardized patient assessment and correla- cessity, accuracy, and reliability of the identified variables
tion of MRI and surgical findings. Although the selection as diagnostic guidelines to differentiate both types of inter-
of MRI variables was based on previously published veteri- vertebral disk herniation.
nary and human neuroradiology studies, it is possible that In summary, this study identified potential clinical and
some of the variables were not necessarily associated with MRI variables to improve differentiation of thoracolum-
a perfect diagnostic accuracy for the intended purpose. For bar intervertebral disk extrusions from protrusions. More
example, assessment of epidural hemorrhage was based on specifically, duration of clinical signs, lateralization of her-
the presence of a poorly demarcated, extradural area of niated disk material, degree of intervertebral disk degen-
heterogeneous intensity on sagittal T2-weighted images,28 eration, presence of multiple intervertebral disk hernia-
which could be considered an unspecific imaging finding. tions, and confinement of herniated disk material to the
Although it is possible that inclusion of gradient echo se- affected intervertebral disk space were identified as inde-
quences would have improved diagnostic accuracy, results pendent variables to predict a diagnosis of intervertebral
of a recent study suggest that identification of a suscepti- disk extrusion or intervertebral disk protrusion. Further
bility artifact on gradient echo spinal MRI studies is also studies are necessary to evaluate the use of these variables
not specific for epidural hemorrhage in dogs with interver- to improve reaching a correct diagnosis of thoracolumbar
tebral disk extrusions.40 It should further be emphasized intervertebral disk extrusion or protrusion.
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