Scorer and modality agreement for the detection of intervertebral disc calcification in Dachshunds

Abstract

Background
The Dachshund is a chondrodystrophic breed of dog predisposed to premature degeneration and calcification, and subsequent herniation, of intervertebral discs (IVDs). This condition is heritable in Dachshunds and breeding candidates are screened for radiographically detectable intervertebral disc calcification (RDIDC), a feature of advanced disc degeneration and a prognostic factor for clinical disease. RDIDC scoring has been previously shown to be consistent within scorers; however, strong scorer effect (subjectivity) was also reported. The aim of this study was to estimate the within- and between-scorer agreement (repeatability and reproducibility, respectively) of computed tomography (CT) scanning and magnetic resonance imaging (MRI) for scoring IVD calcification, and to compare these modalities with radiographic scoring.

Results
Twenty-one Dachshund dogs were screened for IVD calcification using the three imaging modalities. Three scorers scored each case twice, independently. Repeatability was highest for radiography (95.4%), and significantly higher than for CT (90.4%) but not MRI (93.8%). Reproducibility was also highest for radiography (92.9%), but not significantly higher than for CT or MRI (89.4% and 86.4%, respectively). Overall, CT scored IVDs differently than radiography and MRI (64.8% and 62.7% agreement, respectively), while radiography and MRI scored more similarly (85.7% agreement).

Conclusions
Despite high precision for radiography, previous evidence of scorer subjectivity was confirmed, which was not generally observed with CT and MRI. The increased consistency of radiography may be related to prior scorer experience with the modality and RDIDC scoring. This study does not support replacing radiography with CT or MRI to screen for heritable IVD calcification in breeding Dachshunds; however, evaluation of dog-level precision and the accuracy of each modality is recommended.

Full text

Rosenblattetal. Acta Vet Scand (2018) 60:62
https://doi.org/10.1186/s13028-018-0416-2
RESEARCH
Scorer andmodality agreement
forthedetection ofintervertebral disc
calcication inDachshunds
Alana Jayne Rosenblatt1,4*, Anu Katriina Lappalainen2, Nina Alice James1, Natalie Siu Ling Webster3
and Charles Grégoire Bénédict Caraguel1
Abstract
Background: The Dachshund is a chondrodystrophic breed of dog predisposed to premature degeneration and
calcification, and subsequent herniation, of intervertebral discs (IVDs). This condition is heritable in Dachshunds and
breeding candidates are screened for radiographically detectable intervertebral disc calcification (RDIDC), a feature of
advanced disc degeneration and a prognostic factor for clinical disease. RDIDC scoring has been previously shown to
be consistent within scorers; however, strong scorer effect (subjectivity) was also reported. The aim of this study was
to estimate the within- and between-scorer agreement (repeatability and reproducibility, respectively) of computed
tomography (CT) scanning and magnetic resonance imaging (MRI) for scoring IVD calcification, and to compare these
modalities with radiographic scoring.
Results: Twenty-one Dachshund dogs were screened for IVD calcification using the three imaging modalities. Three
scorers scored each case twice, independently. Repeatability was highest for radiography (95.4%), and significantly
higher than for CT (90.4%) but not MRI (93.8%). Reproducibility was also highest for radiography (92.9%), but not
significantly higher than for CT or MRI (89.4% and 86.4%, respectively). Overall, CT scored IVDs differently than radiog-
raphy and MRI (64.8% and 62.7% agreement, respectively), while radiography and MRI scored more similarly (85.7%
agreement).
Conclusions: Despite high precision for radiography, previous evidence of scorer subjectivity was confirmed, which
was not generally observed with CT and MRI. The increased consistency of radiography may be related to prior scorer
experience with the modality and RDIDC scoring. This study does not support replacing radiography with CT or MRI
to screen for heritable IVD calcification in breeding Dachshunds; however, evaluation of dog-level precision and the
accuracy of each modality is recommended.
Keywords: CT, Dachshund, Intervertebral disc calcification, MRI, Radiography, Repeatability, Reproducibility, Scoring
© The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License
(http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium,
provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license,
and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/
publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Background
Of all the dog breeds, the Dachshund has the highest life-
time incidence of intervertebral disc disease (IVDD) [1,
2]. e results of a recent study in the UK, based on a
survey of Dachshund owners (“Dachs-Life 2015”), found
an overall IVDD prevalence of 15.7% in the surveyed
Dachshund population of 1975 dogs, with a significant
prevalence range between different breed variants
(7.1–24.4%) [3]. is high prevalence may be due to a
variety of genetic, physical and lifestyle-related factors
[3], but is likely primarily attributable to their chondro-
dystrophic morphology. Dogs with chondrodystrophy
undergo chrondroid metaplasia, the premature matu-
ration and degeneration of intervertebral discs (IVDs)
that often results in calcification, an indicator of severe
degeneration [2, 4, 5]. ese degenerated IVDs are pre-
disposed to herniate into the spinal canal under minimal
stress, resulting in spinal cord compression and injury
Open Access
Acta Veterinaria Scandinavica
*Correspondence: a.rosenblatt@uq.edu.au
4 Present Address: School of Veterinary Science, The University
of Queensland, Gatton, QLD 4343, Australia
Full list of author information is available at the end of the article

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Rosenblattetal. Acta Vet Scand (2018) 60:62
[4]. Dachshunds with IVD herniation have a high level
of morbidity and mortality, and despite treatment that
often includes complex and costly surgical intervention,
a substantial proportion of dogs retain neurologic deficits
[6–8]. IVDD is widely accepted as the Dachshund breed’s
greatest health problem.
A scheme for radiographic scoring of intervertebral
disc calcification in Dachshunds has been developed,
and recently reviewed [9]. Radiographically detectable
intervertebral disc calcification (RDIDC) is highly her-
itable in Dachshunds [10–14], and the development
of RDIDC at a young adult age corresponds with an
increased risk of developing clinical IVDD during the
lifetime of the dog [8, 10, 15–18]. erefore, screening
young adult breeding candidates for RDIDC, ideally at
24–30months of age, can reduce the prevalence of the
disease in the breed [11, 18, 19]. RDIDC is scored from 0
to a maximum of 26 (i.e. 26 total IVDs in the canine cer-
vical, thoracic and lumbar spine). Current screening pro-
grams recommend that Dachshunds with RDIDC scores
of ≤ 2 are suitable for breeding, dogs with scores of 3–4
should be bred judiciously, and animals with scores ≥ 5
should be excluded for breeding purposes [8, 11, 12, 17,
18].
For a screening test to be useful in a selective breed-
ing program, it must be precise (i.e. very reproducible).
Recent evaluation of within- and between-scorer agree-
ment for RDIDC scoring identified an overall high level
of repeatability and reproducibility, but also identi-
fied some limitations of radiography as a screening tool
[20]. Test precision was influenced by scorer experi-
ence level (expert scorer > specialist radiologi st > gen-
eral practitioner), which in turn affected the consistency
(agreement) of the results. Individual scorer-dependent
subjectivity was also identified.
e absence of RDIDC does not exclude a disc
from being degenerative nor calcified, and only a por-
tion of IVD calcifications present in a spine would be
expected to be detected radiographically [17, 21]. It
is postulated that a cross-sectional imaging modality
such as computed tomography (CT) scanning would
be a superior alternative for screening dogs for IVD
calcification compared to radiography, as CT reduces
challenges associated with anatomic superimposition
and has improved contrast resolution [22, 23]. Alter-
natively, magnetic resonance imaging (MRI) is a cross-
sectional modality with superior contrast resolution to
both CT and radiography, and high-field MRI is con-
sidered the optimal modality for imaging the spine [24,
25]. MRI of intervertebral discs allows identification of
earlier stages of disc degeneration than calcification,
due to its ability to detect biochemical changes in tis-
sues including loss of water and proteoglycan content
and decreased chondroitin-keratan sulfate ratio in the
nucleus pulposus, such that both degenerative and cal-
cified IVDs have decreased MR signal intensity [22,
26–29]. at is, MRI detects a spectrum of IVD degen-
eration but cannot differentiate between calcified and
non-calcified degenerative discs, compared to radiog-
raphy and CT which can only detect disc calcification
as an indicator of (advanced) degeneration. IVD degen-
eration in the canine spine can be reliably graded using
low-field MRI and the Pfirrmann classification system,
which is based on lumbar IVD degeneration in people
and has been verified with the gross pathology-based
ompson system [30–33].
e precision of CT and MRI scoring of IVD calcifi-
cation in Dachshunds has not been assessed. us, the
objectives of this study were to: (i) compare the precision
of three diagnostic imaging modalities (radiography, CT
and MRI) by estimating their repeatability and repro-
ducibility, (ii) estimate and compare the robustness (i.e.
scorer independence) of each modality, and (iii) estimate
the agreement across the three modalities for the detec-
tion of IVD calcification. It was anticipated that both CT
and MRI would be more precise than radiography due to
the cross-sectional nature of these modalities. However, it
was expected that MRI would not completely agree with
the two other modalities because this modality assesses
various stages of IVD degeneration, not only calcification.
Methods
Study subjects
Dogs were prospectively recruited from Finnish Dachs-
hund breeders through e Dachshund Club of Finland,
between 22 November 2011 and 7 March 2012. Eligibility
criteria included: purebred registered Standard Dachs-
hund dog, young adult age (24–48 months old), and
clinically healthy. Dogs were excluded if they had prior
or current signs of intervertebral disc disease (IVDD)
or other illness. Dogs were enrolled in the study with
informed owner consent and the study was approved and
conducted with animal ethics approval.
Diagnostic imaging
e imaging was performed at the University of Hel-
sinki Veterinary Teaching Hospital. ree diagnostic
imaging modalities were employed to image the dogs’
spines—radiography, CT scanning and low-field MRI
(Fig.1). All imaging was performed within a single hos-
pital visit, with the dogs under heavy sedation or gen-
eral anaesthesia. Radiography and CT were conducted
on all dogs, while MRI was optional and based on
owner preference given it would substantially prolong
anaesthetic time for an elective procedure.

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Rosenblattetal. Acta Vet Scand (2018) 60:62
Radiography
Lateral radiographs of the cervical, thoracic and lumbar
spine regions were obtained for each dog using a previ-
ously described protocol [20] and a digital radiographic
system (CPI Indico 100, Ontario, Canada). A minimum
of five diagnostic quality radiographs were acquired for
each dog.
Computed tomography
CT was performed using a 2-slice helical scanner (Sie-
mens Somatom Emotion Duo, Forchheim, Germany) with
the following scan parameters: 100mA, 110kV, 1.0mm
acquisition slice thickness, feed/rotation 2mm, rotation
time 0.8s, reconstruction interval 0.5mm, bone algorithm
(WL, 500; WW, 3500). CT scanner limitations (i.e. excess
tube heat) did not allow for scanning of the entire spine.
e thoracolumbar spine was of greatest interest due to
the propensity for clinical IVDD in this region. ere-
fore, T5-L7 (or a portion thereof) was scanned in all dogs.
Where possible, the cervicothoracic (C6-T2) and/or the
lumbosacral (L7-S1) spine junctions were also scanned;
these regions were selected as they are anecdotally chal-
lenging to score radiographically for IVD calcification due
to issues with superimposition of anatomy.
Magnetic resonance imaging
MRI studies of the thoracolumbar spine were obtained
using a low-field scanner (Vet-MR 0.23T, Esaote S.p.A,
Fig. 1 Example radiographic (a), CT (b, c) and MR (d) images obtained for intervertebral disc (IVD) scoring (not necessarily from the same
Dachshund). The images are centered on the caudal thoracic spine. Example intervertebral disc calcifications are indicated on the lateral spinal
radiograph (a; green arrows), and on the sagittal (b; pink arrows) and transverse (c) CT images which are displayed in a bone window. On the T2W
sagittal MR image (d), the blue arrow indicates an MRI Pfirrmann grade 3 degenerative IVD. CT computed tomography, MRI magnetic resonance
imaging

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Rosenblattetal. Acta Vet Scand (2018) 60:62
Genoa, Italy) and the following pulse sequences: sagittal
plane T1W (TR, 510; TE, 18), sagittal plane T2W (TR,
2800; TE, 80), and transverse plane T1W (TR, 830; TE,
18). As with the CT imaging, the limitations of using a
low-field magnet (specifically, acquisition time) did not
allow for imaging of the entire spine, so the thoracolum-
bar spine (T5-S1, or part thereof) was scanned, being the
region of greatest clinical interest.
Scoring
ree veterinarians who all had diagnostic imaging
backgrounds and training, but varying levels of RDIDC
scoring experience, performed the scoring of the
intervertebral discs. All cases were duplicated, coded
(with individual identifying information removed from
the images), and randomly ordered prior to distribution
to ensure blinding of the scorers. e imaging studies
were viewed in Digital Imaging and Communications
in Medicine (DICOM) format using OsiriX image view-
ing software (Pixmeo, Geneva, Switzerland) and high
resolution/brightness, commercial-grade monitors,
with freedom to post-process images as preferred by the
individual.
Each radiographic study was scored for the presence or
absence of IVD calcification. e CT cases were distrib-
uted 1month after the radiographic scoring had been
completed to facilitate scorer blinding. e subjective
presence or absence of IVD calcification was recorded,
as was scorer confidence in their decision and approxi-
mate percentage of calcification of the total disc cross-
sectional area (in 10% increments, 0–100%). Again, MRI
cases were distributed 1 month after all scorers had
completed the CT scoring. Based primarily on the sagit-
tal T2W images [32], IVDs were graded for any sign of
degeneration (i.e. not specifically calcification) follow-
ing the Pfirrmann classification scheme [30, 33], which
uses visual analysis of the IVD structure, distinction
between nucleus pulposus and annulus fibrosis, MR sig-
nal intensity, and height of the IVD, to grade a disc on
a scale of 1 (normal) to 5 (severe degeneration). Scorers
were provided with example images and written descrip-
tion of the characteristics of each grade, as a reference.
e scorers recorded results for each imaging study
using custom scoring templates, as per a previous study
[20]. Scoring decisions were made by independent opin-
ion. Observers were aware that the dogs were clinically
healthy but were otherwise blinded to patient details and
other identifiers.
Statistical analysis
Scores were collected, collated and formatted using
Microsoft Excel (Microsoft Corporation, Redmond,
WA, USA). An IVD score was classified as positive for
calcification when calcification (≥ 10% of IVD area) was
observed (radiographs and CT) or when the Pfirrmann
grade was ≥ 3 (MRI), and classified as negative otherwise.
Analyses for study objectives (i) and (iii) were conducted
using the statistical package Stata version 14.2 (Stata
Corp, College Station, TX, USA), and analysis for objec-
tive (ii) was conducted using the phylogenetic package
MEGA version 7 [34].
Modalities’ precision (repeatability andreproducibility)
Precision was evaluated by estimating the repeatability and
reproducibility of the three modalities. For a given modal-
ity, repeatability was estimated as the proportion of pairs of
scores that agreed within a given scorer. e reproducibil-
ity was measured as the proportion of pairs of scores that
agreed between two scorers. To compare precision across
modalities, separate datasets and logistic models were
developed for repeatability and reproducibility. e datasets
were reformatted in a long format with each observation
reporting an agreement (coded as “1”) or a disagreement
(coded as “0”) between two scorer iterations for a given dog’s
IVD from a same scorer (repeatability dataset) or from two
separate scorers (reproducibility dataset) of a given modal-
ity. Covariate factors included dog, IVD, modality, and
scorer for each observation. Given that agreement observa-
tions were clustered within IVDs and IVDs were clustered
within dogs, random effects for dog and IVD were added to
the models to account for the lack of independence across
observations. Also, given that the study dogs and their IVDs
were scored up to 6 times by a same scorer (clustered within
scorers), scorer was included as a random effect cross-clas-
sified with dog and IVD. When modeling reproducibility,
models with cross-classified structure could not converge
and the reproducibility was modeled using scorers’ pair,
dog, and IVD random effect without cross-classification.
Repeatability and reproducibility across modalities were
estimated and compared by including modality as a fixed
effect in the respective models.
e direct interpretation of the models’ coefficients
(intercepts and/or effect coefficient), ignoring random
effects, provides cluster-specific estimates of agreement.
To obtain average estimates across dogs, scorers and IVDs
(i.e. population-averaged interpretation), cluster-specific
predicted agreements and the limits of the 95% confi-
dence interval were converted to population-averaged
values using the following approximation formula [35]:
(1)
Prob
agreement≈logit −1

β0+β1Modality
/
√
1
+
0.346
∗
σ2
scorer
+
σ2
dog
+
σ2
IVD


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Rosenblattetal. Acta Vet Scand (2018) 60:62
where β0 is the model intercept coefficient; β1 Modality
is the modality fixed effect (radiography set as default
category); σ2
scorer, σ2
dog and σ2
IVD are the scorer, dog and
IVD within dog random effect variance, respectively; and
logit−1 is the inverse of the logit function (logit−1(x) = 1/
(1+e−x)). Post-regression inferences were two-sided and
adjusted using the Bonferroni method (alpha, set at 5%,
divided by the number of pairwise comparisons between
modalities, alphaBonferroni = 1.7%).
Modalities’ robustness (scorer independence)
e ruggedness of a test is defined as the capacity of the
test to resist expected variation across users [36]. In other
words, ruggedness measures how dependent the out-
come of the test is on the person running or interpret-
ing the test. Here, the ruggedness of each modality was
investigated by determining the existence of scorer sub-
jectivity when interpreting IVDs using a diagnostic imag-
ing test. Similar to a previous report [20] and following
the principle of a cluster analysis, distance-based Neigh-
bor-Joining phylograms were built from an alignment of
IVD scores (IVDs in columns and scoring iterations in
rows) to identify the presence of iteration cluster(s) cor-
responding to distinct scoring patterns. If the two scor-
ing iterations from a same scorer cluster together, there is
evidence that the scoring from this scorer is distinct from
the other scorers. To assess the robustness of the node
linking two iterations together, bootstrap support values
(proportion of resampled trees that include the node of
interest) were generated using bootstrap-resampling
1000 times and reported as a percentage on the nodes of
the original tree [37]. A node with a bootstrap support
value of ≥ 70% was considered robust. e advantage of
this approach is that it accounts for both the quantita-
tive distance and the qualitative pattern across scoring
iterations.
Agreement acrossmodalities
Agreement across modalities was estimated as the pro-
portion of pairs of scores between modalities’ iterations
that agreed within a given scorer. Comparisons between
scorer iterations were ignored to exclude between-scorer
effect. e same data structure, model building, and pop-
ulation-averaged interpretation as for repeatability and
reproducibility were used. Agreement across modalities
was explored across all MRI Pfirrmann grade cut-offs (i.e.
≥ 1 to = 5).
Results
Study subjects
Twenty-one young adult (age range, 26–45 months;
median, 30 months; SD, 4.8 months) Dachshund dogs
were recruited. e study population was relatively
homogeneous, with dogs being intact females (n = 10),
intact males (9), neutered female (1) and neutered male
(1); breed variants being standard long-haired (11) or
standard wire-haired (10); and dogs weighing 7.6–12.6kg
(mean, 9.8kg; SD, 1.3kg).
Precision androbustness ofeach modality
A summary of the score for each available IVD in each
dog, for each scorer, each iteration and each modality, is
presented in Fig.2. Estimates and 95% confidence inter-
vals (95% CI) of repeatability (within-scorer agreement)
and reproducibility (between-scorer agreement) are
reported (Table1).
Radiography
Except for the C2-3 IVD of dogs #4 and #21 (Fig.2), all
26 potential IVDs from the 21 participating dogs (544
IVDs in total) were examined radiographically by each
of the three scorers, two times independently (total, 3264
scores). e repeatability of radiography was slightly
higher than its reproducibility suggesting at first little
scorer effect (Table1). However, the phylogram (distance
tree) of IVD scoring using radiography identified three
clear clusters, corresponding to each individual scorer,
supported by high bootstrap values (> 70%) (Fig.3). is
revealed that each scorer had a scoring pattern that was
unique enough to be discriminated from the other scor-
ers. e length of the branches between two iterations
reflects the amount of disagreement between these itera-
tions (i.e. the shorter the branch length, the stronger the
agreement between two iterations). Within each scorer,
the distance between the iterations of scorer B were
clearly longer than for scorers A and C, showing a lower
repeatability for scorer B. Across scorers, scorer B was
further away from the other two scorers corresponding
to poorer reproducibility for this scorer.
Fig. 2 Scoring alignment of individual intervertebral discs (IVDs) scored (column) by each scorer (A, B and C) for each iteration (1 and 2) and each
modality (X-ray, CT and MRI) (row). The intervertebral discs (IVDs) of each of the 21 participating Dachshund dogs are ordered per their location in
the vertebral column i.e. position 1 (C2-3) to 26 (L7-S1). An “a” codes for a negative score, a “g” codes for a positive score, a “dot” codes for a score that
agrees with the first row (X-ray iteration 1 of scorer A), and a “blank” codes for an absent IVD score due to missing data. “X-ray” denotes radiography;
“CT” denotes computed tomography; “MRI” denotes magnetic resonance imaging
(See figure on next page.)

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Rosenblattetal. Acta Vet Scand (2018) 60:62
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CT-C2
CT-A1
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DOG#21
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CT-A2
CT-B1
CT-B2
CT-C1
MRI-C2
MRI-A1
MRI-A2
MRI-B1
MRI-B2
MRI-C1
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Page 7 of 11
Rosenblattetal. Acta Vet Scand (2018) 60:62
Computed tomography
Only a fraction of the IVDs (range, 8 to 19 per dog) were
scanned using CT, providing a total of 314 IVDs scored.
Overall, a total of 1880 CT scores were obtained from the
six scoring iterations, with four scores missing (Fig. 2).
e reproducibility of CT for scoring IVD calcification
approximated its repeatability, which suggested no scorer
effect (Table1). Indeed, the CT phylogram (Fig.4) indi-
cated no evidence of clear clusters (all bootstrap values
< 70%), confirming a lack of evidence of scorer effect
(subjectivity) with CT. e distances between iterations
within a scorer and between scorers were similar but
long, producing a starfish-shaped tree. is reflects lower
within-scorer agreement (repeatability) across all scorers
compared to radiography, which subsequently resulted in
lower between-scorer agreement (reproducibility).
Magnetic resonance imaging
MRI scans were only available for 11 of the participating
dogs and, at most, 14 IVDs per dog were examined. Over-
all, 142 IVDs were scored with a total of 840 MRI scores
obtained from the six scoring iterations. e repeatabil-
ity of MRI was moderately higher than its reproducibil-
ity (Table1). e MRI phylogram (Fig.5) identified one
strong cluster (bootstrap value 100%) corresponding to
scorer B. is suggested that scorer B’s interpretation
of MR images was significantly different from the other
two scorers (i.e. lower reproducibility for this scorer). e
distance between the iterations within scorer B were also
Table 1 Imaging modalities’ repeatability andreproducibility
Model estimates of the repeatability and reproducibility for intervertebral disc
(IVD) calcication scoring by radiography, computed tomography (CT) and
magnetic resonance imaging (MRI) (interpreted as positive if MRI Prrmann
grade ≥3), with 95% condence intervals reported in brackets. Within a column,
dierent superscript letters indicate signicant dierences between modalities
Modality Repeatability (95% CI) Reproducibility (95% CI)
Radiography 95.4%b (92.4–97.3) 92.9%c (67.8–98.8)
CT 90.4%a (84.8–94.1) 89.4%c (62.8–97.7)
MRI 93.8%a,b (88.9–96.6) 86.4%c (60.4–96.4)
Fig. 3 Phylogram demonstrating the agreement within and
between scorers for radiographic scoring of intervertebral disc (IVD)
calcification in 21 Dachshunds. The length of the branches between
different scorers (A, B, C) represent the disagreement between
scorers. The length of the branches between two scorer iterations
(1, 2) represents the within-scorer disagreement. The scale is based
on the number of differing scores out of the 544 IVDs assessed by an
individual scorer. Numerical bootstrap values indicate strength. Scale
bar = 5 IVD scoring differences
Fig. 4 Phylogram demonstrating the agreement within and
between scorers for computed tomographic (CT) scoring of
intervertebral disc (IVD) calcification. The length of the branches
between two scorer iterations (1, 2), and between each of the three
scorers (A, B, C), represents the within-scorer disagreement and
between-scorer disagreement, respectively. The scale is based on
the number of differing scores out of the 314 IVDs assessed by an
individual scorer. Numerical bootstrap values indicate strength. Scale
bar = 5 IVD scoring differences

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Rosenblattetal. Acta Vet Scand (2018) 60:62
clearly longer compared to the iterations within each of
the other two scorers, reflecting a lower repeatability for
scorer B.
Comparison ofmodalities’ precision
Across the three diagnostic imaging modalities, radi-
ography showed the highest repeatability (95.4%) for
scoring IVD calcification, and was significantly higher
than CT (90.4%) but not significantly higher than MRI
(93.8%) (Table1). ere was no significant difference in
reproducibility across the three modalities; however,
a trend was present with decreasing between-scorer
agreement for radiography, followed by CT and then
MRI (92.9, 89.4 and 86.4%, respectively).
Agreement betweenmodalities
Of all three modalities, considerably more IVD calci-
fication was identified by CT (38.8% of all CT scores
were positive for calcification) than radiography (8.2%
of all radiography scores) and MRI (11.6% of all MRI
scores interpreted at Pfirrmann Grade ≥ 3). Reg ardless
of the Pfirrmann grade cut-off used to binarize data
into a ‘positive’ or ‘negative’ score for IVD calcification,
CT moderately agreed with radiography (approximately
65% agreement) (Table 2). Agreement between MRI
and the other two modalities substantially increased at
the Pfirrmann grade cut-off ≥ 3 and was highest at the
cut-off ≥ 4. However, agreements between modalities at
the cut-offs between ≥ 3 and = 5 approximated. At cut-
off ≥ 4, MRI and radiography agreed 85.4% of the time
(95% CI 80.3–89.3%), while MRI and CT agreed 64.9%
of the time (95% CI 56.5–72.4%).
Discussion
Due to the heritability of IVDD and IVD calcification in
Dachshunds, selective breeding is important to reduce
transmission to offspring [11, 14, 38]. Scoring IVDs for
calcification is a reliable predictor of future IVDD devel-
opment [18], and IVD calcification is currently screened
for using conventional radiography. It was predicted that
CT and MRI would provide better precision (repeat-
ability and reproducibility) and less subjectivity than
radiography when scoring for IVD calcification, as these
cross-sectional imaging modalities reduce the confound-
ing effects of anatomic superimposition and provide
superior contrast resolution [25]. Despite expectations,
neither the repeatability nor reproducibility of CT or
MRI was better than the repeatability and reproducibility
Fig. 5 Phylogram demonstrating the agreement within and
between scorers for magnetic resonance imaging (MRI) scoring of
intervertebral disc (IVD) calcification. The length of the branches
between two scorer iterations (1, 2), and between each of the three
scorers (A, B, C), represents the within-scorer disagreement and
between-scorer disagreement, respectively. The scale is based on
the number of differing scores out of the 142 IVDs assessed by an
individual scorer. Numerical bootstrap values indicate strength. Scale
bar = 2 IVD scoring differences
Table 2 Agreement betweenscoring modalities relative toMRI Prrmann grade cut-o
Model estimates (95% CI) of pairwise agreement between scoring modalities for each MRI Prrmann grade cut-o used to binarize data into a ‘positive’ or ‘negative’
score for intervertebral disc (IVD) calcication
CT computed tomography, MRI magnetic resonance imaging
Compared modalities Prrmann
grade ≥ 1 Prrmann
grade ≥ 2 Prrmann
grade ≥ 3 Prrmann
grade ≥ 4 Prrmann
grade = 5
Radiography vs. CT 64.2% (58.5–69.4) 64.4% (58.5–69.9) 65.6% (58.0–72.5) 67.0% (59.0–74.2) 67.1% (58.9–74.3)
Radiography vs. MRI 20.1% (16.2–24.6) 46.4% (40.1–52.8) 80.8% (75.1–85.4) 85.4% (80.3–89.3) 83.9% (78.4–88.2)
CT vs. MRI 45.9% (39.9–52.0) 51.1% (44.6–57.5) 62.8% (54.8–70.0) 64.9% (56.5–72.4) 62.8% (54.2–70.7)

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Rosenblattetal. Acta Vet Scand (2018) 60:62
of radiography. While the repeatability of MRI was simi-
lar to that of radiography, the repeatability of CT was sig-
nificantly less. e reproducibility of both CT and MRI
were less than that of radiography, however these were
not significantly different. As anticipated for all modali-
ties, estimates of repeatability were higher than estimates
of reproducibility, although the two values were very sim-
ilar for CT. e similar repeatability and reproducibility
for CT indicates a lack of individual scorer subjectivity
for this modality. Challenges with scoring IVD calcifi-
cation using CT could have been due to less experience
and/or training using this method of screening com-
pared to radiography. Further, CT detected substantially
greater overall numbers of calcified IVDs than the other
modalities, including discs with smaller total proportion
of calcification. is may have led to decreased scorer
confidence in assigning a positive or negative score to a
given IVD and thus greater variability between scoring
iterations.
While the repeatability and reproducibility estimates
were similar for both radiography and CT, MRI showed
a larger discrepancy between repeatability and reproduc-
ibility. e lower level of reproducibility for MRI could
be explained by the clear difference in scoring pattern
of scorer B compared to scorers A and C (Fig.5). It is
unclear which of the scorers were scoring most correctly
(i.e. accurately); regardless, it could be concluded that a
degree of difficulty arose when using MRI to screen for
IVD calcification, possibly attributable to a lack of expe-
rience or training using MRI and the Pfirrmann grading
system. On the other hand, our findings are similar to
those of others who have evaluated the reliability of the
Pfirrmann MRI classification system [30, 33, 39]. When
the system was initially evaluated in people, the intra-
and inter-observer agreement yielded average kappa
scores of 0.88 and 0.77, respectively, with percentage
agreements that approximated our results (90.8% and
83.0%, respectively) [33]. A subsequent reliability study
was conducted using a modified Pfirrmann grading sys-
tem, and the intra- and inter-reader agreement remained
good but comparatively less (Avg. K scores, 0.86 and 0.66,
respectively; Avg. % agreement, 84.9% and 66.8%, respec-
tively) [39]. Variable intra- and inter-observer agreement
for scoring canine IVDs for degeneration using the Pfir-
rmann grading system has been identified (K score range,
0.58 to 0.93) [30, 40]. We chose not to use conventional
kappa values because of the recognised limitations of this
method including its sensitivity to prevalence [41], which
limits direct comparison between our agreement esti-
mates and the kappa results obtained in earlier studies.
e Pfirrmann grading system is based on identify-
ing progressive phases of IVD degeneration [30, 33], not
specifically IVD calcification. Although this means that
our estimates of agreement for scoring IVD calcifica-
tion between the different modalities cannot be consid-
ered equal, a cut-off Pfirrmann grade ≥ 3 was selected to
assign a ‘positive’ score for IVD calcification on MRI. We
chose this cut-off as grades of 3, 4 and 5 are assigned to
IVDs with changes (reduced MR signal intensity and dis-
tinction between nucleus pulposus and annulus fibrosus)
that would be expected with more severe IVD degen-
eration, potentially including some degree of calcifica-
tion [32, 42]. Further, it is recognised that discriminating
between Pfirrmann grades 1 and 2, and between grades
3 and 4, can be challenging and subjective [30, 33, 39],
supporting the choice to categorise scores of ≤ 2 as nega-
tive and ≥ 3 as positive for calcification. e agreement
estimates between modalities at cut-off ≥ 3 approximated
those at cut-offs ≥ 4 and = 5 ( Table2).
e recommendation that RDIDC scoring be per-
formed by experts is further supported by the higher
precision found in this study for scorers that had specific
experience in diagnostic imaging, compared to our prior
study using a heterogeneous group of scorers with vari-
able backgrounds [20]. Based on the agreement estimates
identified herein, the chance of every IVD within a given
dog being scored identically when evaluated twice by the
same person (repeatability) is 29.4% (0.95426), compared
to 12.5% seen previously [20]. Similarly for reproduc-
ibility, when a given dog is scored twice by two different
scorers the chance of every IVD within that dog being
identically scored is 14.7% (0.92926), compared to 5.1%.
ese calculations assume complete independence of
individual IVD scoring, which is the worst-case scenario.
Radiography was the only modality of the three to show
a clear scorer pattern (i.e. subjectivity), demonstrated
as three distinct scoring clusters (Fig.3). ese findings
agree with those from our earlier work [20]. e scorer-
dependent patterns demonstrated in that study were
attributed to scorer differences that might be explained
by variation in scoring ability and experience (general
practitioner, specialist radiologist, and expert scorer).
Comparatively, in the present experiment the scorers
had a more similar background and training in diagnos-
tic imaging; therefore, the observed subjectivity is less
likely to be attributed to scorer ability but instead may be
due to distinct individual scoring styles that could feasi-
bly develop with greater experience. Nevertheless, of the
three modalities evaluated, radiography provides con-
sistently higher within- and between-scorer agreement
across all 26 potential IVDs, and when the highest level
of precision in IVD calcification scoring is desired, radi-
ography should be considered above CT and MRI.
e agreement estimates across the three modalities
showed that MRI and radiography agreed more with each
other than CT did with either modality. More agreement

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Rosenblattetal. Acta Vet Scand (2018) 60:62
between radiography and CT might be initially expected as
both modalities assess IVD calcification specifically, whereas
MRI scoring is based on a wider spectrum of IVD degen-
eration. However, the lack of modality agreement between
radiography and CT, and MRI and CT, is likely due to the
substantially larger number of IVD calcifications detected
using CT versus the other two modalities. e potential
benefits of this higher detection rate using CT need fur-
ther investigation. Although the relatively good agreement
between radiography and low-field MRI (85.7%) could make
MRI an acceptable alternative to RDIDC scoring when per-
formed by an individual who is experienced using the Pfir-
rmann grading system, MRI is substantially more expensive
and time consuming to perform than radiography, making it
an impractical screening tool for dog breeders.
e results of this study suggest that further insight into
the accuracy of each modality is required before consid-
ering replacement of radiography with CT or MRI for
IVD calcification screening in Dachshunds. As might be
expected, the three modalities appeared to detect distinct
features of IVD degeneration. While it seems that radi-
ography is the best method of IVD screening in terms of
precision, it is suspected that CT is in fact scoring more
correctly—that is, CT is more accurate—than radiography
and MRI, resulting in the disagreement of CT scores with
radiography and MRI. Use of a modified Pfirrmann grad-
ing system that is more discriminatory in determining
severity of disc degeneration, such as the one developed
for elderly people [39], may be warranted in Dachshunds.
If CT or MRI were shown to be more accurate than radi-
ography, any gains achieved would need to be balanced
with the increased cost, reduced access to the modality in
veterinary practice, and overall feasibility for breeders.
Potential limitations of this study might be related to
the CT and MRI equipment used, as whole dog spines
could not be imaged because of technical limitations,
thereby reducing the number of IVDs that were sampled
and scored. However, the total number of scores obtained
for each modality by the duplicate iterations for each of
three scorers was sufficiently high for analysis at the indi-
vidual IVD level. Analysis of scorer precision at the whole
dog level was not performed due to the aforementioned
limitations. Further, low-field MRI has known limitations
in terms of image quality compared to high-field MRI;
nevertheless, the literature indicates that low-field MRI
is suitable for grading IVD degeneration in dogs [28, 30–
32]. e moderately inconsistent number and position of
IVDs imaged by the various modalities in different dogs
could have caused human counting error when identify-
ing which IVD was being scored at a given time. How-
ever, visual examination of the score summary diagram
(Fig.2) did not identify patterns suggestive of frequent
counting or localisation errors.
Conclusions
While it might be anticipated that more advanced screen-
ing modalities, namely CT and MRI, would improve
diagnosis of IVD calcification compared to radiographic
scoring, this study did not find any improvement in
repeatability or reproducibility of those modalities. If an
alternative modality were to replace radiography, train-
ing in modality-specific scoring should be implemented
to increase within- and between-scorer agreement and
test robustness. With correct scorer instruction, CT and
MRI have the potential to increase the precision of IVD
calcification screening. However, it is important to first
evaluate the accuracy of CT and MRI to provide appro-
priate recommendations regarding which, if any, of the
alternative modalities should replace radiography for the
screening of IVD calcification in Dachshunds.
Abbreviations
CT: computed tomography; IVD: intervertebral disc; IVDD: intervertebral disc
disease; MRI: magnetic resonance imaging; RDIDC: radiographically detectable
intervertebral disc calcification.
Authors’ contributions
AR is the primary investigator, collected data, was a scorer in the study, contrib-
uted to data interpretation, and was a major contributor to manuscript writing.
AL developed the study topic, was the key facilitator in data collection, and
was a scorer in the study. NJ assisted data collation and statistical analysis, and
contributed to manuscript writing. NW was a scorer in the study, contributed
to experimental methodology, and reviewed the manuscript. CC contributed
to study design, performed data analysis and interpretation, and contributed to
manuscript writing. All authors read and approved the final manuscript.
Author details
1 School of Animal and Veterinary Sciences, The University of Adelaide, Rose-
worthy Campus, Adelaide, SA 5005, Australia. 2 Faculty of Veterinary Medicine,
University of Helsinki, Viikki Campus, Agnes Sjöberginkatu 2, 00014 Helsinki,
Finland. 3 Darkroom Veterinary Imaging, 7/489A Warrigal Rd, Moorabbin, VIC
3189, Australia. 4 Present Address: School of Veterinary Science, The University
of Queensland, Gatton, QLD 4343, Australia.
Acknowledgements
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Availability of data and materials
The datasets generated and analysed during the current study will be pub-
lished in the Figshare repository: https ://figsh are.com/s/e5869 b6236 0790c
ff2a0 .
Consent for publication
Not applicable.
Ethics approval and consent to participate
Dogs were enrolled in the study with informed owner consent, and the study
was conducted with ethics approval from the National Animal Experiment
Board of Finland (approval number, ESAVI/5794/04.10.03/2011).
Funding
The authors would like to thank The Faculty of Veterinary Medicine at the
University of Helsinki, The School of Animal and Veterinary Sciences at the
University of Adelaide, and The Dachshund Club of Finland, for their financial
support of the project.

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Rosenblattetal. Acta Vet Scand (2018) 60:62
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in pub-
lished maps and institutional affiliations.
Received: 16 January 2018 Accepted: 3 October 2018
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