Received: 31 July 2017
Revised: 16 November 2017
Accepted: 16 November 2017
DOI: 10.1111/vru.12598
O R I G I N A L I N V E S T I G AT I O N
Comparison between magnetic resonance imaging, computed
tomography, and arthrography to identify artificially induced
cartilage defects of the equine carpal joints
José Suarez Sanchez-Andrade1
Andrea S. Bischofberger2
1 Diagnostic Imaging Clinic, Vetsuisse Fac-
ulty, University of Zurich, CH-8057, Zurich,
Switzerland
Henning Richter1
Patrick R. Kircher1
Karolin Kuhn1
Séamus Hoey3
Abstract
While articular cartilage changes are considered to be one of the initial events in the pathologi-
2 Equine Hospital, Equine Department,
cal cascade leading to osteoarthritis, these changes remain difficult to detect using conventional
Vetsuisse-Faculty, University of Zurich,
CH-8057, Zurich, Switzerland
diagnostic imaging modalities such as plain radiography. The aim of this prospective, experimental,
3 School of Veterinary Medicine, University
College Dublin, Dublin, Ireland
Correspondence
José Suarez Sanchez-Andrade, Diagnostic Imaging Clinic, Vetsuisse Faculty, University of Zurich,
CH-8057, Zurich, Switzerland.
Email: jsuarez@vetclinics.uzh.ch
methods comparison study was to compare the sensitivity of magnetic resonance imaging (MRI),
magnetic resonance arthrography, computed tomography (CT), and CT arthrography in the detection of artificially induced articular cartilage defects in the equine carpal joints. Defects were created in the antebrachiocarpal and middle carpal joint using curettage by a board-certified equine
surgeon. Normal articular cartilage thickness varied from a maximum of 1.22 mm at the level of
the distal aspect of the radius to a minimum of 0.17 mm in the proximal articular surface of the
third carpal bone. Regarding cartilaginous defect measurements the remaining cartilaginous bed
range from a maximum of 0.776 mm in the partial thickness defects, and 0 mm (defect reaches
the subchondral bone) when total thickness defect were made. Computed tomography and magnetic resonance imaging were performed followed by CT arthrography and magnetic resonance
arthrography after antebrachiocarpal and middle carpal intraarticular contrast administration. All
images were reviewed by two board-certified veterinary radiologists, both of whom were blinded
to the location, presence of, and thickness of the cartilage defects. A total number of 72 lesions in
nine limbs were created. Mean sensitivity for localizing cartilage defects varied between imaging
modalities with CT arthrography showing the best sensitivity (69.9%), followed by magnetic resonance arthrography (53.5%), MRI (33.3%), and CT (18.1%) respectively. The addition of contrast
arthrography in both magnetic resonance and CT improved the rate of cartilage lesion detection
although no statistical significance was found. Computed tomographic arthrography displayed
the best sensitivity for detecting articular cartilage defects in the equine antebrachiocarpal and
middle-carpal joints, compared to magnetic resonance arthrography, MRI, and CT.
KEYWORDS
articular cartilage, carpus, direct arthrography, osteoarthritis
1
INTRODUCTION
Degeneration of the articular cartilage is considered a hallmark feature
of osteoarthritis but changes in the articular cartilage remain difficult
In the equine industry, lameness due to joint injury and disease is the
to definitively identify with radiography since this technique does not
most common cause of diminished athletic function in racing horses.
allow direct visualization of cartilage.2–4
Several epidemiologic studies have found that lameness due to joint
Various imaging techniques have been employed in both human
disease is the most significant factor responsible for inability to race
and veterinary medicine in the evaluation of articular cartilage. In
and loss of performance.1 Osteoarthritis is a degenerative inflamma-
humans, magnetic resonance imaging (MRI) has been established as
tory condition in which there is a loss of articular cartilage matrix.
the standard cartilage imaging modality. Magnetic resonance imaging
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Vet Radiol Ultrasound. 2018;59:312–325.
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SUAREZ SANCHEZ-ANDRADE ET AL .
techniques have been developed and optimized to depict cartilage
The use of contrast media in the detection of articular carti-
morphology and allow cartilage volume quantification. The most
lage defects remains controversial and results have shown conflict-
widely used and accurate of these cartilage-specific sequences include
ing conclusions. In horses CT, CT arthrography and MRI have been
spoiled gradient-recalled echo and fast spin-echo imaging.5 Three-
used to detect non-cartilaginous18 and cartilaginous changes of the
dimensional T1-weighted spoiled gradient-recalled echo acquisitions
distal interphalangeal and metacarpophalangeal/metatarsophalangeal
provide high-resolution contiguous thin-slice images in shorter scan
joints.19,20 In one study, the detection of MCP/MTP joint articular car-
times than can conventional spin-echo techniques. Fat-suppressed
tilage pathology was unaffected by the addition of intraarticular con-
spoiled gradient-recalled echo images show high contrast between
trast media to MR or CT studies.18 Conversely, one study found the
bright cartilage and relatively dark fluid, bone, fat, and
muscle.5
Fast
sensitivity and specificity of CT arthrography to be significantly greater
spin-echo imaging of cartilage benefits, in addition, from inherent
compared to 3 Tesla MRI for the detection of articular cartilage defects
magnetization transfer effects within normal cartilage, potentially
in the MCP/MTP joint of horses.20
abnormalities.4,5
Some studies have shown that the areas supporting most of the
Three-dimensional spoiled gradient-recalled echo sequences pro-
stress during locomotion in the equine carpus, especially during hyper-
vide high spatial resolution; however imaging time is relatively long
extension, are located on antebrachiocarpal and middle carpal joints
and three-dimensional spoiled gradient-recalled echo sequences
and particularly the dorsal and medial aspects. The carpometacarpal
are particularly sensitive to motion and susceptibility artifacts and
joint remains stationary under plane axial and torsional loading and
previous intraarticular surgery may produce moderate amounts of
therefore has lower importance in terms of the mechanical properties
susceptibility artifacts in these sequences.5 Both intermediate- and
related to motion and loading.21,22
increasing the relative conspicuity of cartilage
T2-weighted fast spin-echo imaging sequences, with and with- out
The objective of this study was to determine the sensitivity of MRI,
fat suppression, have been advocated in the assessment of articular
magnetic resonance arthrography, CT and CT arthrography techniques
cartilage integrity.5 Proton density–weighted and T2-weighted fast
for the detection of artificially induced articular cartilage defects in
SE imaging techniques are well suited for morphologic assessments of
eight clinically relevant anatomic regions of the equine antebrachio-
articular cartilage as well as menisci and ligamentous structures, pro-
carpal and middle carpal joints. Our hypothesis was that CT arthrog-
viding information of a quality comparable to that obtained in surgery.
raphy and magnetic resonance arthrography techniques would show
T1-weighted images show intra-substance anatomic detail of hyaline
the highest sensitivity values in the detection of articular cartilage
cartilage but do not provide good contrast between joint effusion
lesions, followed by MRI and CT. It was furthermore hypothesized that
and the cartilage surface, a shortcoming that limits their usefulness
the addition of intraarticular contrast media would improve the rate
in the assessment of focal cartilaginous
defects.6,7
In one MRI study
of the equine carpus, cartilage measurements obtained in sequences
of detection of the cartilage defects compared to the nonenhanced
studies.
such as spoiled gradient-recalled echo with and without fat saturation
techniques have shown excellent agreement with histomorphometric
measurements.8 The main advantage of computed tomography (CT)
2
MATERIALS AND METHODS
over MR is improved spatial and temporal resolution.9 Computed
tomography is still nowadays the modality of choice for evaluation of
The study was a prospective, experimental, methods comparison
thin cortical bone changes or subtle calcifications. In contrast, CT has
design. The distal limbs of five adult horses (one Paso Fino and four
inferior soft tissues contrast resolution compared to MR9 allowing
Warmbloods) with a median age of 17 years (range of 12–23 years)
poor differentiation between synovial fluid and articular cartilage.
were collected within 12 h of euthanasia at the Equine Hospital,
The intraarticular injection of contrast media in MR and CT have
Vetsuisse-Faculty, University of Zürich for reasons unrelated to the
been shown to help in outlining capsular and ligamentous structures
study. Since this was a cadaveric study no animal permission was
as well as the joint cartilage. As such magnetic resonance arthrography
needed. Sample size was reached based on a consensus of the non-
and computed tomography arthrography procedures can be utilized
blinded authors, who considered that 80 defects (10 joints with eight
in the assessment of intraarticular ligamentous structures, menisci,
defects per joint) examined by two blinded observers would result in
osteochondral lesions and loose bodies.10,11 Arthrography can be per-
a number with sufficient statistical power. All horses had no history
formed using various different contrast media including gas, saline, iod-
of lameness associated with the carpus at the time of euthanasia, this
inated contrast or Gadolinium based contrast media or a combination.
lack of carpal lameness was the inclusion criteria for the study. After
Computed tomographic arthrography allows the cartilaginous eval-
euthanasia, all limbs were isolated from the body at the level of the
uation of the entire joint,12 rather than constrained to areas perpen-
distal diaphysis of the radius, stored at –28◦ C, and identified with a
dicular to the acquisition plane as in conventional magnetic resonance
number. As required, specimens were thawed to room temperature,
arthrography.13 Several studies performed in the human knee, ankle
clipped, and cleaned before the arthroscopic procedure.
and shoulder comparing CT arthrography techniques with magnetic
resonance arthrography and arthroscopic findings have shown that CT
arthrography is an accurate, sensitive and specific technique in the
2.1
Arthroscopy protocol
evaluation of cartilage thickness,14,15 surface cartilage lesions, and car-
Arthroscopy examination of the antebrachiocarpal and middle carpal
tilage loss.16,17
joints was performed by means of a standard dorsal approach23 by
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SUAREZ SANCHEZ-ANDRADE ET AL .
a board certified veterinary surgeon (A.B.). Articular cartilage defects
for the presence or absence of defects in the aforementioned locations
were created with variably sized curettes (Karl StorzTM size 0 and 00)
in the carpal joints. Both of the observers were blinded to the presence,
and located as follows: one each at the level of the medial and lateral
location, number, and the characteristics of the defects in contrast to
radial facets, one each at the proximal and distal articular surfaces of
the other authors. Each observer was asked to review the studies for
the intermediate and radial carpal bones as well as two at the proxi-
evidence of cartilaginous defects beginning with CT followed by the
mal articular surface of the third carpal bone (3CB); one at the level
MRI, CT arthrography, and magnetic resonance arthrography respec-
of the radial facet; and another one at the level of the intermediate
tively. All horses were completely randomized by means of random
facet, respectively (Figure 1). Defect size, shape, and depth (full or par-
permutation and anonymized for avoiding bias during the examination
tial thickness) varied and were randomly determined by the surgeon.
of the images. Reviewers were permitted to alter the window level and
The arthroscopic portals were closed in two layers: the joint capsule
width, zoom, and evaluate any of the sequences within the individual
with a single cruciate suture using United States Pharmacopeia 2-0 gly-
study (CT, MR, CT arthrography, or magnetic resonance arthrography).
comer suture and the skin in a simple interrupted pattern using United
A defect was described as a discontinuity in the surface of the articu-
States Pharmacopeia 2-0 polybutester suture. Following arthroscopy
lar cartilage with interruption of its smooth surface. Cartilage appear-
all limbs were frozen at –28◦ C and scanned within the next 2 weeks.
ance varied between the different sequences, from the hypointense
appearance compared to the synovial fluid in the T2 and the proton
2.2
Imaging protocol
density sequences to the slightly more hyperintense appearance compared to synovial fluid in the T1 images. In the CT arthrography images
The limbs were thawed over 12–18 h and subsequently imaged using
the defect was defined as a focal irregular in shape defect on the artic-
a multidetector 16 Slice CT (Philips 16 Brilliance. Philips AG, Zurich,
ular surface that was filled with contrast media. In the plain CT studies
Switzerland) in helical mode acquisition at a 0.8 mm slice thickness,
recognition of the irregularity created by the defect represented the
with a pitch of 1, 120 kVp, 100 mAs, a display field of view of 250 mm,
most challenging aspect.
matrix of 768 × 768 and in both medium and high frequency reconstruction algorithms. Immediately post CT examination, an MRI examination of all limbs was performed using a 3 Tesla magnet (Philips
Ingenia, Philips AG, Zurich, Switzerland) using a surface coil (Philips
Medical Systems, Best, The Netherlands). Magnetic resonance imaging sequences, planes and acquisition parameters are summarized in
Table 1.
To formulate a combined contrast medium for both CT arthrography and magnetic resonance arthrography, iohexol and gadolinium
were combined. For arthrography, as there is no established consensus in veterinary medicine on component contrast media concentrations, our technique was based on previously published human reference values.16 The aim was to reach a final iohexol concentration of
150 mgI/ml and gadolinium to solution ratio of 1:200. As such 300
mgI/ml iohexol (GE Healthcare. Accupaque 300 mgI/ml) was diluted in
1:1 ratio with 0.9% NaCl saline. Then, an adapted volume of gadolinium contrast based media (GE Healthcare. Omniscan 0.5 mmol/ml) was
added to obtain a final gado:sol ratio of 1:200. The antebrachiocarpal
and the middle carpal joints were injected with 30 and 20 ml of this mix-
2.4
Gross analysis
Limbs were carefully dissected by one of the authors (J.S.S.); the distal
radius and individual carpal bones were disarticulated and stored for
further analysis. Thin sections were acquired through the defects
of the distal radius and carpal bones using an anatomic band saw
and scanned using a flatbed color image scanner (Epson Perfection
V700 Photo scanner) at a resolution of 800 dpi (dots per inch). The
minimal articular cartilage thickness was measured and recorded
by the same author with a dedicated open source image processing
software designed for scientific multidimensional image (ImageJ 2.0.0,
National Institute of Health, Bethesda, MD, USA) analysis at the level
of each defect (measurements represent the remaining cartilaginous
bed after the arthroscopic procedure) but also the unaffected cartilage
adjacent to the defect, to establish the normal cartilage thickness of
the location.
2.5
Statistical analysis
ture, respectively, a magnetic resonance arthrography was performed
The statistical parameters included in the study were decided by con-
including T1W turbo field echo three dimensional and T1W turbo
sensus by two of the authors (H.R. and J.S.S.). All data were statistically
spin echo sequences. Finally a CT arthrography study was conducted
analyzed using a commercial software package (IBM SPSS Statistics for
using the previously described CT protocol. Time elapsed between the
Windows, version 21.0, IBM Corp. Armonk, NY, USA). Based on the
intraarticular injection of contrast media and the magnetic resonance
study design and the examined sample number, the data distribution
arthrography was less than 1 min and between magnetic resonance
was not assumed to be normal. Sensitivity values and 95% confidence
arthrography and CT arthrography was between 5 and 10 min.
interval were calculated by considering gross analysis as the reference
for each of the different imaging modalities. Interobserver agreement
2.3
Image analysis
was calculated by means of nonweight kappa (k) statistics. Nonparametric tests (Friedman and Wilcoxon) were performed to analyze data
Images were reviewed independently by two board certified radiolo-
between all modalities. P < 0.05 was considered significant. Negative
gists with 7 (S.H.) and 9 (K.K.) years of experience using a diagnostic
controls were not established in the study design; consequently speci-
workstation (Mac OS X Yosemite. 2.66 GHz Intel Core 2 Duo. Apple,
ficity, positive predictive value, negative predictive value, and accuracy
CA, USA) and a dedicated medical imaging software (Horos v2.0.0 RC5)
could not be calculated.
SUAREZ SANCHEZ-ANDRADE ET AL .
315
F I G U R E 1 Sagittal (A) and dorsal (B) computed tomographic arthrography multiplanar reconstructed images of a defect located at the level the
lateral facet of the distal articular surface of the radius (arrows) and the corresponding gross image of the sagittal section made through the defect
(C). In (A) and (B) contrast media is noted within the antebrachio carpal and middle carpal joints and filling the focal indentation in the articular
surface that represent the artificially performed defect. Moderate amount of air is visible within the periarticular soft tissues as well as within the
carpal joints. Air was unavoidably introduced during the arthoscopic procedure [Color figure can be viewed at wileyonlinelibrary.com]
316
SUAREZ SANCHEZ-ANDRADE ET AL .
TA B L E 1
Scanning parameters of the magnetic resonance imaging sequences used in the study
T2W TSE
PD
T1W TSE
T1W TFE
Plane
Sagittal, dorsal
Sagittal
Sagittal, transverse
3D
Reconstructed Voxel size
0.25 × 0.31 mm
0.40 × 0.45 mm
0.25 × 0.31 mm
0.40 × 0.40 × 0.60 mm
Slice thickness
1.5 mm
2.0 mm
2.0 mm
0.6 mm
FOV
120 × 120 × 102 mm
120 × 120 × 107 mm
110 × 110 × 101 mm
160 × 160 × 130 mm
Matrix
344 × 270
300 × 256
3126 × 250
268 × 268
TR
6950
3120
600
13
100
30
9
6
Freq offset
TE
220 Hz
Averages
2
3
2
1
Interslice gap
1.5 mm
2.0 mm
2.0 mm
–
Flip Angle
90
90
90
8
Fat Sat
No
SPIR
No
No
Contrast
Pre
Pre
Pre/Post
Pre/Post
TSE, turbo spin echo; PD, proton density; TFE, turbo field echo; FOV, field of view; TR, time to repeat; TE, time to echo; Fat Sat, fat saturation.
3
RESULTS
between CT arthrography and MRI, and between CT arthrography
and CT.
A total number of 72 defects were created in the antebrachiocarpal
Finally, the addition of contrast media improve lesion detection as
and middle carpal joints and reviewed by the two, board-certified vet-
more defects were detected in the post contrast studies compared
erinary radiologists (Figures 2–6). One of the limbs was inadvertently
to the plain studies (Table 2); however no statistical significance was
lost during the study time period. The mean sensitivity values for
found between the mean sensitivity values of all modalities, in con-
each technique and the interobserver agreement for both observers
trast with our second hypothesis. When results were analyzed for
are summarized in the Table 2. Computed tomography arthrography
observer 1, there was not a significant difference between magnetic
showed the highest sensitivity in lesion detection (69.9%), followed
resonance arthrography and MRI (P = 0.237), between CT and mag-
by magnetic resonance arthrography (53.5%), MRI (33.3%), and CT
netic resonance arthrography (P = 0.170), and between CT arthrogra-
(18.1%). For both observers CT arthrography displayed the best sen-
phy and magnetic resonance arthrography (P = 0.178), significant sta-
sitivity for lesion detection followed by magnetic resonance arthrog-
tistical differences were noted for observer 1 between CT arthrogra-
raphy, MRI, and CT according to our first hypothesis. When sensitivity
phy and MRI (P = 0.023) and CT arthrography and CT (P = 0.005) as
results were break down for observer 1 and 2, the maximum sensitiv-
well as for all modalities for observer 2.
ity for lesion detection was seen also for CT arthrography (observer 1:
Based on the measurements obtained with the dedicated open
55.6%, observer 2: 84.5%). In none of the techniques all lesions were
source image processing software on the sagittal cuts of the carpal
detected. The comparison between the gross analysis and the detec-
bones and radius normal cartilage thickness varied depending on the
tion rate showed high significant differences for all modalities in lesion
location from a maximum height of 1.22 mm in the distal aspect of
identification. Comparison between gross analysis and imaging modal-
the radius to a minimum of 0.17 mm in the radial facet of the third
ities was only related to the presence or absence of a lesion.
carpal bone. The cartilage thickness at the created defects ranged from
Friedman tests, performed to detect differences in lesion detection across multiple modalities, were highly significant (P < 0.001).
0.776 mm of the remaining cartilage bed thickness in partial-thickness
defects to an absence of cartilage in full-thickness defects.
Table 3 summarizes the P-values between modalities for the detection
rate of the two observers. For observer 1, the comparison of detection rate between modalities showed significant differences between
4
DISCUSSION
CT arthrography and MRI (P = 0.023) and between CT arthrography
and CT (P = 0.005). For observer 2, significance could be detected
The best results in detection of articular cartilage defects of the equine
between all modalities. Agreement between MRI and magnetic res-
antebrachiocarpal and middle carpal joints were achieved with CT
onance arthrography was k = 0.253 (fair) for observer 1 and k =
arthrography followed by magnetic resonance arthrography, MRI, and
0.264 (fair) for observer 2 respectively. Agreement between CT and CT
CT in agreement with our hypothesis.
arthrography was k = 0.052 (slight) for observer 1 and k = 0.136 (slight)
for observer 2.
The higher spatial resolution of CT arthrography associated with
the high contrast between the low density of cartilage and the highly
For observer 1 and 2 significance differences were noted between
attenuating intraarticular iodine allows a better confidence level in
modalities at several sites (Table 4). For both observers, signifi-
the diagnosis of cartilage lesions compared to MRI and MR arthrog-
cant differences were noted at the proximal radial carpal bones
raphy. This is in agreement with previous studies in human medicine
SUAREZ SANCHEZ-ANDRADE ET AL .
317
F I G U R E 2 Sagittal T1 weighted turbo field echo magnetic resonance arthrography (A) and Dorsal T2 weighted magnetic resonance imaging
(B) images depicting a defect on the proximal articular surface of the third carpal bone. In (A) contrast media is visible within the periarticular
soft tissues dorsal to the carpal joints as well within the antebrachio carpal and middle carpal joints filling the joints spaces, whereas in (B) the
hyperintense synovial fluid highlights the lesions. An additional defect can be seen in the lateral aspect of the distal articular surface of the radius
in (B) (dotted arrows). Corresponding gross (C) image of the lesion in the third carpal bone [Color figure can be viewed at wileyonlinelibrary.com]
318
SUAREZ SANCHEZ-ANDRADE ET AL .
F I G U R E 3 Sagittal computed tomographic arthrography multiplanar reconstructed image (A) showing a defect on the distal articular surface of
the radial carpal bone (white arrow) with its corresponding gross image (C). Dorsal computed tomographic arthrography image (B) showing two
lesions; one located on the proximal articular surface of the intermediate carpal bone (black arrow) with its corresponding scanned gross image (D).
The white dotted arrow highlights a defect on the proximal articular surface of the radial carpal bone. Defects are seen as focal indentations on the
thin hypoattenuating line that represents the articular cartilage. The asterisk in (B) represents an artifact likely due to volume averaging since no
defects were present at that location [Color figure can be viewed at wileyonlinelibrary.com]
SUAREZ SANCHEZ-ANDRADE ET AL .
319
F I G U R E 4 Sagittal T1 weighted turbo fast echo magnetic resonance arthrography (A) and dorsal CTA (B) images demonstrating a defect (arrows)
on the medial aspect of the proximal articular surface of the third carpal bone. Real defect thickness (C) and size (D) can be seen in the in the scanned
gross images. Cartilaginous defect in this case measured 0.37 mm in thickness [Color figure can be viewed at wileyonlinelibrary.com]
320
SUAREZ SANCHEZ-ANDRADE ET AL .
F I G U R E 5 Sagittal T2 weighted magnetic resonance imaging (A) and T1 weighted turbo spin echo magnetic resonance arthrography (B) images
showing a defect (arrows) on the proximal articular surface of the intermediate carpal bone. One can notice the hyperintense synovial fluid in the T2
weighted image (A) and the hyperintense appearance of the contrast media in the T1 weighted image (B) filling the focal indentation on the articular
surface that represents the artificially induced defect. Bottom images represent the gross scanned intermediate carpal bone, sagittal cut (C) and
entire bone (D). Articular cartilage thickness adjacent to the defect was in this case 0.88 mm [Color figure can be viewed at wileyonlinelibrary.com]
SUAREZ SANCHEZ-ANDRADE ET AL .
321
F I G U R E 6 Transverse computed tomography images showing the approximate location (red crosses) where the board certified surgeon performed the articular defects. Location is approximate since defects were randomly performed and defect location was not always the same in terms
of laterality. One can also appreciate the gas present between the carpal bones and periarticular soft tissues introduced during the arthroscopic
procedure [Color figure can be viewed at wileyonlinelibrary.com]
evaluating the usefulness of CT arthrography in the assessment
The low interobserver agreement displayed for all the techniques,
of joints with thin articular cartilage. Furthermore CT arthrography is
especially between CT arthrography and CT, as well as the low sen-
considered in human medicine the most accurate method in evaluating
sitivity may be explained by the several limitations of the current
cartilage thickness, in the settings of research studies.14–16 In this
study design and imaging modalities. In this study each observer was
regard CT arthrography is more accurate than cartilage specific
a board-certified radiologist with 7 and 9 years of experience in the
MRI sequences such as spoiled gradient-recalled echo as well as MR
evaluation of equine imaging, plus the more large animal based train-
arthrography, as shown by cadaveric studies on the human ankle15 and
ing of observer 1 in relation to observer 2. We must recognize that
the hip,14 respectively. A statistical significant difference was found
interobserver agreement is fundamentally affected by the ability of
between CT arthrography and magnetic resonance arthrography (P =
an observer to identify defects, which may be associated with fac-
0.002) using the same contrast media.
tors such as experience and confidence in identifying subtle findings.
322
SUAREZ SANCHEZ-ANDRADE ET AL .
TA B L E 2 Lesion detection (sensitivity) for all modalities
(computed tomography, computed tomographic arthrography, magnetic resonance imaging, and magnetic resonance arthrography) of
both observers and interobserver agreement (k)
equate in further characterization of the defects into partial or full
thickness in any of the imaging modalities. As such it was not feasible to analyze full- or partial thickness defects separately or make an
attempt to correlate gross measurements of the cartilage with mea-
CT
CTA
MRI
MRA
Observer 1
34.7%
55.6%
36.1%
45.8%
our institution and with few papers in veterinary medicine describing
Observer 2
1.4%
84.5%
30.6%
61.1%
CT arthrography and magnetic resonance arthrography appearance of
Mean Sensitivity
18.1%
69.9%
33.3%
53.5%
the equine articular cartilage, therefore image interpretation of such
surements from the imaging modalities. Magnetic resonance arthrog-
Sensitivity
raphy and CT arthrography techniques are not performed routinely at
Inter-observer agreement (*)
0.052
0.136
0.253
0.264
*Significant at P < 0.05.
CT, computed tomography; CTA, computed tomographic arthrography;
MRI, magnetic resonance imaging; MRA, magnetic resonance arthrography.
studies has some inherent difficulties. During the arthroscopic procedure a moderate amount of gas was inadvertently but unavoidably
introduced into the joint space creating magnetic susceptibility artifacts in the subsequent imaging studies and thus the interpretation of
the images was made more difficult compared to the more normal clini-
Without separation of the adjacent articular surfaces due to intraar-
cal circumstances since some of these gas bubbles may be located adja-
ticular fluid administration, defect detection with CT alone seems
cent to the artificially created defects and therefore obscuring them.
unlikely. We choose to include CT, even knowing its limited value in
Considering the ex vivo nature of this study and that after collection, all
cartilage evaluation, because we decided to have pre- and postcontrast
specimens were frozen for a variable period prior to imaging, it is possi-
studies in CT and also in MRI.
ble that postmortem change and freeze–thaw effects could have led to
This low interobserver agreement in lesion detection and the low
worsening of artifacts identified on cross-sectional imaging studies.28
number of limbs in the study may also explain the not significantly
These artifacts include decrease contrast between different tissues
differences between modalities in lesion detection. However sensi-
when temperature is around 0◦ C29 or a central signal reduction arte-
tivities and the degree of agreement were always the highest in the
fact, resembling an isotherm distribution.30 Therefore subtle inade-
postcontrast studies independently of the observer. Based on
quacies in core specimen thawing can lead to an initially confusing pat-
the results of the sensitivities displayed in Table 2, we postulate that
tern of central signal dampening; however none of these changes were
the addition of contrast media is superior to the plain studies but it is
detected in any of our examinations. A combination of these reasons
limited by the interobserver variation.
may partially explain why the observers did not detect many of the
Based on the measurements acquired adjacent to the cartilaginous
lesions the normal articular cartilage thickness in the antebrachio-
defects and similarly why there was a lower interobserver agreement
in lesion detection.
carpal and middle carpal joints is very thin, ranging from 0.17 mm
The rounded conformation of the equine antebrachiocarpal and
at the level of the proximal articular surface of the third carpal
middle carpal joints can also act as a limiting factor in the detection of
bone to 1.2 mm at the level of the radial articular facets. There-
lesions. The limitations of spatial resolution of the imaging modalities
fore, the spatial and contrast resolution pose a greater limitation in
used, leading to volume averaging are made worse by the curved struc-
the equine carpus than for other regions such as the human knee,
tures. The use of unique plane images may have led to volume averag-
where articular cartilage is 5–6 mm25 and thus is considerably thicker
ing affecting lesion identification, except for the limited slices oriented
than the cartilage of the antebrachiocarpal and middle carpal joints.
perpendicular to the joint surface.31 The equine carpal joints represent
Even the equine distal interphalangeal joint had areas with cartilage
a more complex anatomic area compared to the distal interphalangeal
two to three times thicker17 than previously reported in the equine
or metacarpophalangeal joints; including thinner cartilage, a more
metacarpophalangeal26 or carpal27 joints. Due to the thin cartilaginous
rounded articular surface, and multiple small bones forming the joints,
coverage in all equine carpal joints, differences in thickness between
all of which affect the spatial resolution of MRI and CT imaging.19,26,27
partial and full-thickness defects resulted in only a few hundreds of
Limitations due to cartilage thickness have been already describe in a
micrometers. It is described that pixel size has to be at least three
previous human study which evaluated the efficacy of MRI in detect-
times smaller than the cartilage thickness to identify three cartilage
ing articular cartilage defects of the wrist and conclude that MRI is rel-
laminae.8,26 The achievable spatial resolution of the MRI and magnetic
atively inaccurate for detecting and allowing description of focal artic-
resonance arthrography sequences used in the study as well as the
ular cartilage defects in the radiocarpal joint.24 As a result, we limited
minimal spatial resolution of the CT protocols was considered inad-
evaluation to the detection of or absence of defects and attempts at
TA B L E 3
Wilcoxon signed ranks test of lesion detection between modalities for both observers
CT vs. MRI
CT vs. MRA
Observer 1
0.862
0.170
Observer 2
<0.001*
<0.001*
CTA vs. CT
CTA vs. MRI
0.005*
0.023*
<0.001*
<0.001*
CTA vs. MRA
MRA vs. MRI
0.178
0.237
0.002*
<0.001*
*Significant at P < 0.05.
CT, computed tomography; CTA, computed tomographic arthrography; MRI, magnetic resonance imaging; MRA, magnetic resonance arthrography.
323
SUAREZ SANCHEZ-ANDRADE ET AL .
TA B L E 4
Obs1
Obs2
Comparison between detection rate for each modality at the different locations with the P-values of comparisons between modalities
MRA vs. MRI
CT vs. MRI
CTA vs. MRI
CT vs. MRA
CTA vs. MRA
CTA vs. CT
RAD
22.2 vs. 22.2%
44.4 vs. 22.2%
33.3 vs. 22.2%
44.4 vs. 22.2%
33.3 vs. 22.2%
33.3 × 44.4%
Lat
1.000
0.317
0.655
0.317
0.655
0.564
RAD
22.2 vs. 66.7%
33.3 vs. 66.7%
55.6 vs. 66.7%
33.3 vs. 22.2%
55.6 vs. 22.2%
55.6 vs. 33.3%
Med
0.102
0.257
0.655
0.655
0.083
0.317
RCB
66.7 vs. 55.6%
33.3 vs. 55.6%
100 vs. 55.6%
33.3 vs. 66.7%
100 vs. 66.7%
100 vs. 33.3%
Prox
0.564
0.317
0.046*
0.083
0.083
0.014*
RCB
44.4 vs. 33.3%
44.4 vs. 33.3%
55.6 vs. 33.3%
44.4 vs. 44.4%
55.6 vs. 44.4%
55.6 × 44.4%
Dist
0.655
0.655
0.317
1.000
0.655
0.655
ICB
88.9 vs. 55.6%
66.7 vs. 55.6%
77.8 vs. 55.6%
66.7 vs. 88.9%
77.8 vs. 88.9%
77.8 vs. 66.7%
Prox
0.180
0.655
0.414
0.317
0.564
0.655
ICB
44.4 vs. 33.3%
22.2 vs. 33.3%
44.4 vs. 33.3%
22.2 vs. 44.4%
44.4 vs. 44.4%
44.4 × 22.2%
Dist
0.655
0.655
0.655
0.317
1.000
0.317
3CB
66.7 vs. 0%
11.1 vs. 0%
44.4 vs. 0%
11.1 vs. 66.7%
44.4 vs. 66.7%
44.4 vs. 11.1%
Lat
0.014*
0.317
0.046*
0.025*
0.317
0.083
3CB
11.1 vs. 22.2%
22 vs. 22.2%
33.3 vs. 22.2%
22.2 vs. 11.1%
33.3 vs. 11.1%
33.3 × 22.2%
Med
0.655
1.000
0.655
0.655
0.157
0.655
RAD
66.6 vs. 33.3%
0 vs. 33.3%
100 vs. 33.3%
0 vs. 66.7%
100 vs. 66.7%
100 vs. 0%
Lat
0.083
0.083
0.014*
0.014*
0.083
0.003*
RAD
55.6 vs. 77.8%
0 × 77.8%
88.9 vs. 77.8%
0 × 77.8%
88.9 vs. 55.6%
88.9 vs. 0%
Med
0.414
0.008*
0.655
0.025*
0.180
0.005*
RCB
66.7 vs. 22.2%
11.1 vs. 22.2%
100 vs. 22.2%
11.1 vs. 66.7%
100 vs. 66.7%
100 vs. 11.1%
Prox
0.046*
0.655
0.008*
0.025*
0.083
0.005*
RCB
44.4 vs. 33.3%
0 vs. 33.3%
100 vs. 33.3%
0 vs. 44.4%
100 vs. 44.4%
100 vs. 0%
Dist
0.655
0.083
0.014*
0.046*
0.025*
0.003*
ICB
77.8 vs. 22.2%
0 vs. 22.2%
100 vs. 22.2%
0 vs. 77.8%
100 vs. 77.8%
100 vs. 0%
Prox
0.025*
0.157
0.008*
0.008*
0.157
0.003*
ICB
88.9 vs. 22.2%
0 vs. 22.2%
88.9 vs. 22.2%
0 vs. 88.9%
88.9 vs. 88.9%
88.9 vs. 0%
Dist
0.034*
0.157
0.034*
0.005*
1.000
0.005*
3CB
77.8 vs. 0%
0 vs. 0%
77.8 vs. 0%
0 vs. 77.8%
77.8 vs. 77.8%
77.8 vs. 0%
Lat
0.008*
1.000
0.008*
0.008*
1.000
0.008*
3CB
11.1 vs. 33.3%
0 vs. 33.3%
11.1 vs. 33.3%
0 vs. 33.3%
11.1 vs. 11.1%
11.1 vs. 0%
Med
0.157
0.083
0.157
0.083
1.000
0.317
*Significant at P < 0.05.
MRI, magnetic resonance imaging; CT, computed tomography; MRA, magnetic resonance arthrography; CTA, computed tomographic arthrography; RAD,
radial bone facet; RCB, radial carpal bone; ICB, intermediate carpal bone; 3CB, third carpal bone.
differentiation between full and partial cartilaginous defects were not
sition times at high resolution and higher sensitivity to susceptibility
undertaken.
artifacts.26,35 Apart from the fat saturation techniques, also the gra-
The sequences in our MRI protocol were chosen as they have been
dient echo MR sequences, named turbo field echo in our protocol,
previously described in the literature to be effective for evaluation
may have affected image interpretation. Magnetic susceptibility arti-
of articular cartilage in both veterinary and human medicine.32–34
fact results in signal loss and distortion due to magnetic field inhomo-
The MRI parameters are reflective of the parameters used for equine
geneity and occurs at tissue interfaces, such as where bone and soft
orthopedic MRI at our institution and acquisition times of all the
tissue meet.
sequences used here were considered acceptable for clinical use,
Our study was designed for the use of a single contrast agent for
since the overall time of the imaging protocol for the MRI including the
all imaging modalities aiming for its use in a clinical situation regard-
postcontrast was around 70 min. With short TE and a low flip angle,
less of the modality employed and allowing multiple modalities to be
proton density and T1 effects predominate, which result, particularly
used with a single intraarticular injection. In MRI, the use of other con-
cartilage.26
trast media such as saline solution may have facilitated detection of
Some limitations of the fat saturation techniques include longer acqui-
articular cartilage pathology in the T1 fast field echo or proton density
when fat suppression is applied, in very bright hyaline
324
SUAREZ SANCHEZ-ANDRADE ET AL .
sequences, as the ideal contrast agent for the sequences used would be
hypointense to the articular cartilage rather than isointense.33 While it
is possible to achieve similar joint distension with saline and gadolinium, the imaging characteristics of intra- articular gadolinium confer
Category 2
(a) Drafting the Article: Suárez J, Hoey S, Richter H
(b) Revising Article for Intellectual Content: Suárez J, Richter H,
Kuhn K, Bischofberger AS, Kircher PR, Hoey S
certain advantages over saline. While saline is inert and inexpensive,
intraarticular saline and any intraarticular or periarticular fluid collection will be of similar signal intensities36 making the differentiation between them impossible. Some authors report an interaction
Category 3
(a) Final Approval of the Completed Article: Suárez J, Richter H,
between iodinated contrast and gadopentetate dimeglumine and sug-
Kuhn K, Bischofberger AS, Kircher PR, Hoey S
gested that iodinated contrast diminished the ability of gadopentetate
dimeglumine to shorten T1 relaxation times in high concentrations.37
Jinkins et al.38 found that iodinated contrast agents themselves have a
ORCID
Andrea S. Bischofberger
http://orcid.org/0000-0002-7623-8627
weak T1 shortening effect that results in higher signal intensity than
water as seen on T1-weighted sequences, thus making the differentiation between contrast media and cartilage more difficult. Another
study describes how following intraarticular injection of gadolinium
and iodinated contrast, authors occasionally observed suboptimal contrast on T1-weighted images and low signal intensity of synovial fluid
on T2-weighted images, both on high-field and low-field strength systems and concluded that mixture of gadolinium with iodinated contrast
might affect gadolinium enhancement and reduce image quality.39
Thus it may be possible that the mixture of contrast media used with
a concentration of almost 50% iodine was not ideal for the magnetic
resonance arthrography studies. One study shows that a mixture of
1.25 mmol/l gadolinium and 25% iodinated contrast agent is optimal
for simultaneous magnetic resonance arthrography and CT arthrography in vitro.40 They further recommend that to decrease the signal
loss of additive iodine, an iodinated contrast agent concentration of
more than 37.5% should not be used for simultaneous magnetic resonance arthrography and CT arthrography; however the use of lower
concentrations of iodinated contrast may result in lower contrast viscosities that would enhance the delineations of small intraarticular
structural irregularities.41 It is possible that altering the protocol to
include modified magnetic resonance image sequence parameters, use
of a different contrast media, such as saline or a lower concentration
of iodine in the final mixture, may improve the utility of MRI and/or CT
arthrography.
In conclusion, CT arthrography showed the best sensitivity in the
detection of articular cartilage lesions of the equine antebrachiocarpal
and middle carpal joints followed by magnetic resonance arthrography,
MRI, and CT. The addition of contrast media did improve the detection
of the lesions however no statistical significant difference was found
between modalities.
LIST OF AUTHOR CONTRIBUTION
Category 1
(a) Conception and Design: Suárez J, Hoey S, Bischofberger A,
Kircher PR
(b) Acquisition of Data: Suárez J, Hoey S, Kuhn K
(c) Analysis and Interpretation of Data: Suárez J, Hoey S, Kuhn
K, Richter H
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