COMPARISONS AMONG RADIOGRAPHY, ULTRASONOGRAPHY

AND COMPUTED TOMOGRAPHY FOR EX VIVO CHARACTERIZATION

OF STIFLE OSTEOARTHRITIS IN THE HORSE

JULIE DE LASALLE, KATE ALEXANDER, JULIEN OLIVE , SHEILA LAVERTY

A better understanding of imaging characteristics of equine stifle osteoarthritis (OA) may allow earlier
detection and improve prognosis. Objectives of this ex vivo, prospective, methods comparison study were
to (1) describe the location and severity of naturally acquired OA lesions in the equine stifle using ultrasound
(US), radiography (XR), computed tomography (CT), and macroscopic evaluation (ME); (2) compare the
diagnostic performance of each imaging modality with ME; and (3) describe subchondral bone mineral density
(BMD) in equine stifle joints with OA using CT. Radiographic, CT, and US evaluations were performed on
23 equine cadaver stifles and compared with ME. Significant associations were found between osteophyte global
scores for all imaging modalities (CT, P ˂ 0.0001; XR, P = 0.005; US, P = 0.04) vs. ME osteophyte global
scores. Osteophytes were detected most frequently in the medial femorotibial (MFT) joint. A specific pattern
of osteophytes was observed, with a long ridge of new bone at the insertion of the MFT joint capsule cranially
on the medial femoral condyle. A novel caudo-10°proximo-5°lateral-cranio-disto-medial oblique radiographic
projection was helpful for detection of intercondylar osteophytes. Multiplanar CT reformatted images were
helpful for characterizing all osteophytes. Osteophyte grades at most sites did not differ among modalities.
Low sensitivity/specificity for subchondral bone sclerosis and flattening of femoral condyles suggested that
these signs may not be reliable radiographic and CT indicators of equine stifle OA. Equine stifle OA was
associated with a decrease in BMD and specific sites of focal subchondral bone resorption/cyst formation
were found in some specimens.  C 2016 American College of Veterinary Radiology.

Key words: computed tomography, equine, imaging, osteoarthritis, stifle.

Introduction supraphysiological, joint loads may lead to OA. Confor-

O STEOARTHRITIS (OA) IS A FREQUENT cause of poor
performance in horses and has been estimated to
represent more than 50% of all lameness problems.1,2 It
is well recognized that repetitive intense or single impact,
From the Department of Clinical Sciences, Faculty of Veteri-
nary Medicine, University of Montreal, 3200 Sicotte, PO Box 5000,
Saint-Hyacinthe, QC, Canada (De Lasalle, Alexander, Olive, Laverty)
Comparative Orthopedic Research Laboratory, Faculty of Veterinary
Medicine, University of Montreal, 3200 Sicotte, PO Box 5000, Saint-
Hyacinthe, J2S 7C6, QC, Canada (De Lasalle, Laverty).
Funding sources: Supported by grants from the Association des
Vétérinaires Équins du Québec (AVEQ) and the Pfizer Animal Health
Fund. Sheila Laverty’s Comparative Orthopedic Research Laboratory
is currently funded by the National Sciences and Engineering Council
of Canada (NSERC), Fonds de Recherche Santé Quebec FRSQ Réseau
THÉCell, and also by a donation from Mr. and Mrs. John Magnier,
Coolmore Stud, Fethard, Co Tipperary, Ireland.
Previous presentations or abstracts: One abstract was presented as an
oral presentation and one as a poster at the 2014 ACVR Annual Scientific
Meeting, St. Louis, Missouri, USA.
Address correspondence and reprint requests to Julie De Lasalle,
Department of Clinical Sciences, Faculty of Veterinary Medicine, Uni-
versity of Montreal, 3200 Sicotte, PO Box 5000, Saint-Hyacinthe, QC,
J2S 7C6, Canada. E-mail: julie.de.la.salle@umontreal.ca
Received May 24, 2015; accepted for publication January 28, 2016.
doi: 10.1111/vru.12370
mation also has a role in the development of tarsal OA.
However, there is sparse information on the etiology or
epidemiology of equine femorotibial OA.3–7 A variety of
causes have been identified for femorotibial OA including
soft tissue injury and instability such as medial collateral or
cranial cruciate injury.8–10 Meniscal damage is also a com-
mon cause of femorotibial OA.11–13 Other causes such as
subchondral cyst also contribute to the pathology.6
The stifle is a large, high motion joint and one of the
most complex joints in the horse. A recent study estimated
that stifle lesions in equine athletes may account for more
than 40% of hindlimb injuries.14 However, the exact preva-
lence of OA in the equine stifle remains unknown. Although
some authors have reported a prevalence as low as 3% of
stifle lameness, this prevalence increased in older horses
and athletes and is reported by others to be as high as 32%
of all stifle diseases.10,11,15 The prognosis has anecdotally
been considered to be poor.11,16,17 Additionally, studies are
lacking regarding the clinical significance of radiographic
signs of femorotibial OA in horses.18,19
Vet Radiol Ultrasound, Vol. 00, No. 0, 2016, pp 1–13.

1
2 DE LASALLE ET AL.
Although radiographic abnormalities related to OA
of the equine stifle have been described mainly as pe-
riarticular osteophytes, subchondral bone abnormalities
are also an integral part of the disease.7,20 Flattening
of the articular surfaces, narrowing of the femorotibial
joint space, sclerosis of the subchondral bone, and/or lu-
cent zones in the subchondral bone are reported radio-
graphic features of equine stifle OA.16 These lesions are
mostly described in the medial compartment of femorotib-
ial joint.16,21 Anatomy of equine stifle has been described
using computed tomography (CT) and MRI.22–26 Natu-
rally acquired stifle OA lesions have only been mentioned
with ultrasound (US) and CT, described with low-field
MRI and briefly arthroscopically and not reported with
macroscopic evaluation (ME).12,17,27–29 Assessment of bone
mineral density (BMD) using CT has been reported in
equine metacarpophalangeal OA.30,31 Bone mineral den-
sity has been calculated on healthy equine stifles using dual-
energy X-ray absorptiometry (DEXA) but never in equine
stifle OA.32
We hypothesized (1) that osteophytes would be located
at specific sites primarily in the medial femorotibial (MFT)
joint, (2) that CT would permit detection of a greater num-
ber of smaller osteophytes than other modalities, (3) that
subchondral bone sclerosis and an increase BMD would be
associated with OA, and (4) flattening of femoral condyles
would not be associated with OA. The objectives of this
ex vivo prospective study were to (1) describe the location
and severity of OA lesions in the equine stifle with US, XR,
CT, and ME, to (2) compare the diagnostic performance of
each imaging modality relative to ME and to (3) quantita-
tively assess the subchondral BMD in the equine stifle OA
using CT. By comparing each imaging modality, this may
change the diagnostic approach and help management of
clinical cases. The ultimate goal of this study was to bet-
ter characterize equine stifle OA to be able to recommend
appropriate imaging in order to obtain an accurate diagno-
sis, which may lead to a better response to treatment and
possibly improve prognosis.
Methods
The study was a prospective, ex vivo, descriptive, and
methods comparison design. Abbreviations and terms used
in the study are listed in Appendix A1.
Sample Selection Procedures
Screening radiographs were acquired for a total of 77
stifles, using horses from a local abattoir or from hospital
patients euthanized for reasons unrelated to the project.
For each stifle, one caudo-cranial projection was made us-
ing a 10" × 12 " computed radiography (XR) plate (Agfa,
2016
CR HD5.0 General, Agfa CR DX System, Toronto, ON,
Canada) and 80–85 kVP and 15–25 mAs technique settings.
Screening radiographs were made either standing prior to
euthanasia, within 6 h postmortem or on frozen joints. Each
screening radiograph was assessed by a veterinary radiolo-
gist (KA) and graded based on a subjective grading system
of femorotibial OA (absent (0), mild (1), moderate (2), and
severe (3)) adapted from Cohen.17 Stifles were selected for
inclusion in the study if they were skeletally mature and
had radiographic signs of OA (grades 1, 2, and 3). For fi-
nancial reasons and to ensure statistical independence in
the samples, only one stifle per horse was included in the
study, with the exception of two stifles that were from the
same horse. Additional normal stifles were randomly ex-
cluded from the study population. Stifles with osteochon-
dritis dissecans and/or fracture were also excluded. Within
36 h postmortem, each limb selected for the study was sec-
tioned at mid-femur and mid-tibia, and the caudal muscles
were resected while keeping the joint capsule intact. All
joints were wrapped in moist towels and plastic and frozen
at −20°C.
Ultrasonography Procedures
Limbs were thawed at 4°C for 24–48 h preceding multi-
modality imaging. Each joint underwent two-dimensional
gray scale US (Digital Ultrasonic Diagnostic Imaging Sys-
tem, MindRay, DP-6600Vet, Vet Novations Canada Inc.,
Barrie, ON) in a water bath with a 7.5 MHz linear trans-
ducer.
Computed Tomography Procedures
Before CT image acquisition, each specimen was
placed in a 35-l heavy plastic impermeable bag that was
filled with water in order to mimic the muscle mass
normally surrounding the stifle. Each limb was placed
in lateral recumbency on a solid dipotassium phosphate
(K2 HPO4 ) reference phantom (Cann-Genant 13002 Model
3 CT Calibration Phantom, Mindways Software, Inc.,
San Francisco, CA). Each joint underwent CT using a
third-generation, 16-slice helical CT scanner (HiSpeed
ZXi, General Electric, Mississauga, Ontario, Canada)
and the following protocol: 120 kVp and 350 mA, slice
thickness 1.25 mm, slice interval 1.25 mm, pitch 0.625:1,
display field-of-view 25 cm and including the entire
reference phantom, speed 6.25 mm/rotation, number of
rotations 1/s, matrix 512 × 512, pixel size 0.49 mm and
reconstructed with a high-pass (bone) algorithm. Each set
of CT images was reformatted in sagittal and dorsal planes
at an image interval of 1 mm and in three-dimensional
(3D), generating a total of four image series per joint.
VOL. 00, NO. 0 IMAGING OF EQUINE STIFLE OA 3

FIG. 1. Three-dimensional reformatted CT images illustrating 15 anatomic locations (with defined abbreviations) that were evaluated using three imaging
modalities and macroscopic examination for each of 23 equine stifle joints. Exceptions were as follows: MFE, LFE, and CrT were not evaluated macroscopically;
ICF, MICE, LICE were not evaluated with US; and subchondral bone sclerosis was not evaluated on the patella, femoral epicondyles, and femoral trochlear
ridges. (A) Cranial view of one equine stifle joint used in the study (lateral is to the left).
1. PP: proximal part of patella,
2. DP: distal part of patella,
3. MP: medial part of patella,
4. LFE: lateral femoral epicondyle,
5. LFC: lateral femoral condyle,
6. LFTR: lateral femoral trochlear ridge,
7. MFTR: medial femoral trochlear ridge,
8. MFE: medial femoral epicondyle,
9. MFC: medial femoral condyle,
10. LTP: lateral tibial plateau,
11. LICE: lateral intercondylar eminence,
12. MICE: medial intercondylar eminence,
13. MTP: medial tibial plateau,
14. CrT: cranial part of tibia.
(B) Dorsal planar slice focused on the femoral intercondylar region (lateral is to the left).
15. IF: femoral intercondylar fossa.

Radiography Procedures each specimen and modality. Radiographic and CT find-

Each joint underwent computed XR while still in
the water-filled bag. The limbs were oriented vertically,
without pressure, with the femur proximally, in order
to mimic a standing position. Four projections were
made: latero-medial (LM), caudo-60°lateral-craniomedial
oblique (Ca60L-CrMO), caudo-60°medial-craniolateral
oblique (Ca60M-CrLO), and caudo-10°proximo-5°lateral-
cranio-disto-medial oblique (Ca10Pr5L-CrDiMO) which
replaced the standard Ca10Pr-CrDiO for better assessment
of the intercondylar region.
Image Evaluation
Specimens were divided into 15 sites (Fig. 1) for CT and
XR evaluation, based on prior descriptions of the distribu-
tion of OA lesions in stifles of other species.33–35 Presence
of marginal osteophytes was recorded using a semiquan-
titative scoring system to assess severity. As with the ra-
diographic screening procedure, osteophytes were graded
at each site as absent (0), mild (1), moderate (2), and se-
vere (3) based on a subjective grading system of femorotib-
ial OA adapted from Cohen.17 Individual sites were also
summed in order to obtain an osteophyte global score for
ings were recorded independently by two veterinary radi-
ologists (KA, JO) (10 and 3 years of experience) who were
unaware of macroscopic OA status. Scores from the second
radiologist were only used for interobserver comparisons.
Images were analyzed using a dedicated diagnostic work-
station (Advantage Workstation AW 4.3, General Electric,
Mississauga Healthcare). The radiographic projection or
CT plane where osteophytes were most visible was also
noted. Ultrasonographic evaluation of osteophytes (defined
as abnormal bony irregularities on articular margins) was
performed at 12 sites by a veterinary radiology graduate
student with 5 years’ experience in equine practice (JDL)
who was unaware of macroscopic OA status. Three of the 15
sites that could not be adequately evaluated with US were
the intercondylar fossa of femur (ICF) and medial and lat-
eral intercondylar eminences of tibia (MICE, LICE). Each
osteophyte site was evaluated in transverse and longitudinal
ultrasonographic planes.
In addition to osteophytes, observers also recorded
femoral and tibial subchondral bone sclerosis on dorsal
CT images and on caudo-cranial XR (Ca10Pr5L-CrDiMO)
projections. Sclerosis was defined as an increase in sub-
chondral bone mineral opacity on XR and as an increase
4 DE LASALLE ET AL. 2016

FIG. 2. Computed tomographic images illustrating the technique used for bone mineral density (BMD) calculations. (A) The stifle was positioned lateral
side down on a calibration phantom containing five parallel rods of known physical density. Computed tomography images were acquired helically, using slice
locations illustrated on the dorsal reformatted image (E). On medial and lateral femoral condyles, slices at 10 mm (B), 7.5 mm (C), and 5 mm (D) depths
from the most distal aspect of the condyles were used for density measurements. On medial and lateral tibial condyles, slices at 8.75 mm (F), 6.25 mm (G),
and 3.75 mm (H) depths from the articular surface were used. On each slice, two circular 10 mm2 regions of interest (ROIs) were drawn on the medial and
lateral condyles of both the distal femoral and the proximal tibial bones. Using the phantom as a reference, the mean attenuation value for each ROI was then
converted to BMD.30

in subchondral bone attenuation on CT. Score severity was
based on a semiquantitative evaluation of sclerotis area
(XR) or volume (CT; grade 0: absent, grade 1: less than
10%, grade 2: 10–25%, grade 3: over 25%). Flattening of
femoral condyles was recorded as present (1) or absent
(0) on CT and XR. Observers also recorded presence of
subchondral bone defects/lysis, soft tissue mineralization,
bone irregularities, fragments, or other abnormalities for
all modalities.
Subchondral BMD Measurement
Subchondral BMD was assessed quantitatively in the
femoral and tibial condyles by a single evaluator (vet-
erinary radiology graduate student (JDL)). For each
specimen, BMD was calculated in four areas (lat-
eral femoral condyle (LFC), medial femoral condyle
(MFC), lateral tibial plateau (LTP), medial tibial plateau
(MTP)) within a circular 100 mm2 region of inter-
est (ROI), as previously described, that excluded adja-
cent cortical bone and at depths of 3.75, 6.25, 8.75
mm from the most distal aspect of femur and 5, 7.5,
10 mm from the most proximal aspect of tibia (Fig. 2).36
Then, bone ROI Hounsfield units were converted into
K2HPO4-equivalent BMD values (mg/ml) according to
a linear regression, using ROI values obtained from the
reference phantom.36
Macroscopic Evaluation Procedures
After image acquisition, soft tissues were carefully dis-
sected from the joint for ME. During preparation, all carti-
lage surfaces were kept moist with NaCl 0.9% solution. The
macroscopic findings were recorded based on a consensus
between a veterinary surgeon (SL) with extensive experi-
ence in OA lesion assessment and the veterinary radiology
graduate student (JDL). Twelve of the 15 anatomic sites
were evaluated for marginal osteophytes, employing the
same grading system as that used for imaging (0–3). Three
sites (LFE, MFE, and CrT)) could not be adequately evalu-
ated at ME because of soft tissue attachment. The scores for
the most severe osteophyte at each site were summed in or-
der to obtain an ME osteophyte global score for each stifle
(Fig. 3). The articular cartilage of the distal femur, proximal
tibia, and patella was assessed following the application of
India ink (20% dilution in phosphate buffered saline, pH
7.4 (Design Higgins waterproof drawing ink, black India
4415, Eberhard Faber, Lewisburg, TN), as described previ-
ously for the presence of fibrillation or erosion in the same
12 anatomic locations. Each cartilage lesion was classified
based on a semiquantitative grading system (0–3): grade
0: smooth and regular cartilage; grade 1: mildly irregular
surface without ink staining; grade 2: partial thickness ero-
sion and intense ink staining macroscopically; and grade
3: full-thickness erosion and visualization of the subchon-
dral bone with staining peripheral to the ulceration.37,38
The most severe cartilage lesion scores at each site were
summed to provide an ME cartilage global score for each
stifle. The ME osteophyte global score was then added to
the ME cartilage global score to calculate the ME global
OA score. The ME global OA score was then used to deter-
mine the ME final diagnosis for each stifle as OA positive
(OA+) or OA negative (OA−).
VOL. 00, NO. 0 IMAGING OF EQUINE STIFLE OA 5

FIG. 3. Graph illustrating the technique used for determining macroscopic examination (ME) final diagnosis (OA+ or OA−) for each of the 23 stifle joints
based on the ME global OA score (ME osteophyte global score (red) + ME cartilage global score (blue)). The distribution of ME global OA scores showed two
rather distinct groupings: above and below 15 (green line). The six OA positive specimens were defined as those for which the ME global OA score was equal or
greater than 15. The maximum ME global OA score for one specimen would be 72 (grade 3 osteophytes for all 12 sites added to grade 3 cartilage lesions for all
12 sites). Note that all specimens had cartilage lesions (some were thought to be “wear and tear”) and no specimen had osteophytes without cartilage lesions.

Statistical Analysis toir) presenting definitive or suspected radiographic signs of

OA and six normal specimens (five from teaching hospital
Statistical analyses were selected and performed by a
and one from the abattoir) were retained as negative con-
statistician (GB). Osteophyte severity was compared be-
trols, which was approximately proportional to the number
tween anatomic sites and between imaging modalities and
of specimens in each grade. A definitive OA positive or neg-
ME, using the Cochran-Mantel-Haenszel test. Linear re-
ative classification was then made on all specimens based on
gression analysis was used to evaluate the relationship
their ME global OA score. The distribution of ME global
between osteophyte global score of each imaging modality
OA scores revealed two rather distinct groups: above and
and both ME global OA score and ME osteophyte global
below a score value of 15 (Fig. 3). Six of the 17 screened
score. Global osteophyte scores for XR and CT were also
OA+ specimens had an ME global OA score equal or supe-
compared between observers using a Bland-Altman test
rior to 15 and were definitively classified as OA+. All other
for bias. Sensitivity/specificity and confidence interval of
specimens (the 11 remaining screened OA+ or suspected
femoral condyle flattening and subchondral bone sclerosis
and all screened OA−) were definitively classified OA−.
were determined relative to the ME final diagnosis (OA+
The six OA− at screening had a low ME global OA score
and OA−). Femoral condyle flattening and subchondral
(11 or less). Signalment was known for 14/23 specimens.
bone sclerosis were also compared between observers with
The median age of those 14 stifles was 9.5 years (range 3
a weighted Kappa test. Bone mineral density for each depth
–27 years) and was from various breeds: Quarter Horse (n
and each anatomic site was compared with ME global OA
= 8), pony (n = 3), Appendix (n = 2), Haflinger (n = 1). Six
score using linear regression analysis. For every statistical
were females, six were geldings, and two were intact males.
test, alpha threshold was fixed at 0.05.

Results Locations and severity of OA lesions among modalities

Specimens
From the 77 stifles collected for radiographic screening,
23 specimens were retained for the main study based on the
following selection criteria: 17 equine cadaver stifles (nine
from the equine teaching hospital and eight from the abat-
Osteophytes. All 23 specimens were evaluated with US,
XR, CT, and ME with the exception of four speci-
mens that were not evaluated by US because the ul-
trasonographer was not available on the day of evalua-
tion. Osteophytes were mostly located in the MFT joint,
6 DE LASALLE ET AL.
FIG. 4. Graph illustrating the number of specimens with at least 1 osteophyte (grade 1, 2, or 3) at each of the 15 anatomic sites with different imaging
modalities (US, CT, XR) and macroscopic evaluation (ME). Note that MICE, LICE, and ICF were not evaluated with US. Also, LFE, MFE, and CrT were
not evaluated with ME.
specifically on the MFC and MTP with all modalities and
ME (Fig. 4). In addition, osteophytes were frequently ob-
served on the MICE and intercondylar fossa (ICF) with
XR, CT, and ME (sites not evaluated with US). All of
the medial joint sites presented the most severe osteophyte
scores: grade 3 osteophytes were seen on the MFC with all
modalities and ME, on the MTP with XR and CT, in the
ICF with CT and ME and on the MICE with XR, CT, and
ME. Osteophyte grades at each site did not significantly
differ between modalities except for the medial femoral
trochlear ridge (MFTR) where grades were higher with US
than XR (P = 0.008) and CT (P = 0.008) and for the MFC
where grades were higher with US than XR (P = 0.01),
CT (P = 0.046), and ME (P = 0.0009). Grades were also
higher with CT than ME for the MFC (P = 0.02) and MTP
(P = 0.01). For the MICE, grades were higher with CT
(P = 0.005) and XR (P = 0.02) than ME.
Osteophytes were best observed on two radiographic pro-
jections; the Ca10Pr5L-CrDiMO and the Ca60M-CrLO.
The Ca10Pr5L-CrDiMO revealed intercondylar region os-
teophytes (Fig. 5F). Also, on this projection, two speci-
mens presented a line superimposed on the MFC that cor-
responded macroscopically with a ridge of osteophytes that
extended cranially, just distal to the MFTR (Fig. 5F). The
Ca60M-CrLO showed this same ridge at the cranial aspect
of the MFC in seven specimens (Fig. 5H, dotted arrow). In
addition, the Ca60M-CrLO was useful for the detection of
osteophytes on the cranial aspect of the MTP (Fig. 5H, ar-
rowhead). The Ca60L-CrMO revealed osteophytes on the
caudal aspect of MTP (Fig. 5G). Finally, the LM projection
showed rare osteophytes on the proximal or distal patella
2016
(Fig. 5E). On CT, osteophytes were best observed on
the dorsal plane (Fig. 5J) and 3D reformatting (Fig. 5L)
demonstrated osteophyte distribution, particularly on the
ridge of the MFC. The sagittal plane showed osteophytes
on the caudal aspect of the MTP (Fig. 5K) and the trans-
verse plane showed the extent of osteophytes on the MTP
and the MFC (Fig. 5I).
There was a significant (P = 0.03) mean difference in
osteophyte global score between evaluators with XR of
−2.17, or 4.82% of the maximum possible score of 45 with
Bland-Altman. This bias was independent of grades (P =
0.86). With CT, there was also a significant (P = 0.02) mean
difference in osteophyte global score between evaluators of
−6.13, or 13.6%, which is 2.8 times higher than with XR.
This bias increased with grade severity (P = 0.04). It should
be noted that the observer with lower scores was the one
used for XR and CT comparisons with ME.
Cartilage lesions. Eight specimens had cartilage lesions
alone, without osteophytes, at ME. However, cartilage le-
sions were all graded 1 (possible) except for one specimen
which presented with two grade 2 cartilage lesions.
Flattening of femoral condyles. Medial femoral condyle
flattening was observed on nine specimens with XR and
eight specimens with CT. Compared to the ME global OA
score, MFC flattening had a sensitivity of 33.3% with both
imaging modalities and a specificity of 58.8% with XR and
64.7% with CT. Interobserver agreement for MFC flatten-
ing with a weighted Kappa was 0.34 (fair) with XR and 0.53
(moderate) with CT. Lateral femoral condyle flattening was
not observed.39
VOL. 00, NO. 0 IMAGING OF EQUINE STIFLE OA 7

FIG. 5. Images illustrating ultrasonographic (US), radiographic (XR), and computed tomographic (CT) characteristics of equine stifle joint OA. Five of the
23 stifles are represented. Lateral or dorsal is to the left for all images. Ultrasound images oriented in the longitudinal plane illustrate a grade 1 osteophyte on
DP (arrow) (A) and on the distal portion of LFTR (arrow) (B); and a grade 2 osteophyte on the MTP (arrow) (C) and MFC (arrow) (D). A lateromedial XR
projection (E) shows a grade 1 osteophyte (arrow) at the distal aspect of the patella. A Ca10Pr5L-CrDiMO XR projection (F) shows grade 3 osteophytes on
MICE (white arrow), MTP (black arrowhead), MFC (white arrowhead), and a focal zone of subchondral bone resorption on the craniomedial part of MTP
(black arrow). Note the superimposed line on MFC (dotted arrow) representing the ridge of osteophytes extending cranially and caudally. A Ca60L-CrMO XR
projection (G) shows a grade 3 osteophyte on MTP (arrowhead). A Ca60M-CrLO XR projection (H) shows a grade 3 osteophyte on the cranial part of MFC
(dotted arrow) and on the cranial part of MTP (arrowhead). A transverse CT image (I) shows a grade 3 osteophyte (arrow) on the cranial aspect of the MFC.
A dorsal planar CT image (J) shows a grade 3 osteophyte on MICE (arrow) and MFC (white arrowhead), a grade 2 osteophyte on MTP (black arrowhead)
and a focal zone of subchondral bone resorption on craniomedial part of MTP (black arrow). A sagittal planar CT image (K) shows a grade 2 osteophyte on
the caudal part of MTP (arrowhead). A three-dimensional reformatted CT image (L) shows a grade 3 osteophyte as a large ridge of new bone (black dotted
arrow) on MFC.

Subchondral bone sclerosis. Medial tibial plateau sub-
chondral sclerosis was observed in five specimens with CT
and three specimens with XR, two of which were noted with
CT. Compared with the ME global OA score, subchondral
sclerosis had a sensitivity of 0% with XR and 16.7% with
CT and a specificity of 82.4% with XR and 76.5% with CT.
The interobserver agreement for MTP subchondral scle-
rosis with weighted Kappa was 0.13 with XR and 0.12
with CT. Subchondral sclerosis was not observed on the
MFC.
8 DE LASALLE ET AL. 2016

FIG. 6. Images illustrating CT, XR, and ME characteristics of a central subchondral osteophyte (CO) in one of the stifle joints. (A) Dorsal multiplanar CT
image showing an area of mineralization on the distal surface of the medial femoral condyle (MFC) (arrow). This lesion was not visible in the corresponding XR
image (B). A cartilage “bump” was observed macroscopically on the MFC (arrow) and a corresponding cartilage defect was visible on the MTP (arrowhead).

FIG. 7. Multiplanar reformatted CT images illustrating the appearance of vascular channels and subchondral bone resorption on the tibial plateau. Normal
vascular channels are noted on the distal cranial (E and F) and caudal (A and B) portions of the tibial plateau. Mild (C–G) and severe (D–H) subchondral
bone resorption lesions are also depicted (arrows). Images D and H are from the same stifle joint as that illustrated in Fig. 5D, F, G, H, J.

Subchondral bone resorption. A small cyst was noted with
CT on the MFC of one specimen. This lesion was noted
as flattening of MFC on XR. Also, on CT evaluation, sev-
eral specimens (n = 7) presented a well-defined hypoat-
tenuating focus of variable size with regular to irregular
margins compatible with bone resorption in the subchon-
dral bone. This bone resorption focus was located on the
medial aspect of the MTP, just cranial or caudal to the
intercondylar region and/or on the medial aspect of LFC
(in the region of the origin of the cranial cruciate liga-
ment; Fig. 7C, D, G, H). Five of these seven specimens
were from the six OA+ (higher ME global OA score). One
of these specimens presenting with a severe subchondral
lesion on the cranial aspect of the MTP also presented a
tear in the cranial horn of medial meniscus extending to
the cranial meniscotibial ligament on ME (Figs. 5F–J and
6D–H). Almost all other specimens (of the 16/23) pre-
sented a pattern of two well-defined hypoattenuating tubu-
lar structures similar to vascular channels; one on the cran-
iomedial part of MTP and the other on caudomedial part
on MTP (Fig. 7A, B, E, F). These observations were not
noted on the initial radiographic assessments. Radiographic
assessment was retrospectively repeated in these specimens
to better characterize these lesions. Two of these cystic le-
sions were visible as ill-defined radiolucent foci with irreg-
ular margins on the medial portion of MTP and two were
suspected and corresponded with CT observations. A sim-
ilar lesion was also suspected in the intercondylar fossa ra-
diographically and this specimen presented a subchondral
lesion on medial portion of LFC at CT examination.
Additional lesions. Some additional lesions were ob-
served. One specimen presented a small punctate focus of
mineralization continuous with the subchondral bone on
VOL. 00, NO. 0 IMAGING OF EQUINE STIFLE OA 9

TABLE 1. Mean Osteophyte Global Score Obtained by Specimen with Each Modality

Relationship with ME Relationship with ME

Global OA Score (Osteophytes Osteophyte Global Score
Mean Osteophyte Global and Cartilage Lesions) (Osteophytes Only)
Score by Modality (±SD) P R2 P R2
US 2.83 (±2.01) P = 0.25 7.6% P = 0.04∗ 21.9%
XR 3.39 (±3.35) P = 0.01∗ 27.2% P = 0.005∗ 32.2%
CT 3.96 (±3.40) P = 0.003∗ 34.7% P ˂ 0.0001∗ 52.8%
ME 3.00 (±4.22)

US, ultrasound; XR, radiography; CT, computed tomography; ME, macroscopic evaluation; SD, standard deviation.
Macroscopic evaluation global osteoarthritis score (ME global OA score) and macroscopic evaluation osteophyte global score (ME osteophyte global
score) significance (P: P value; ∗: significant) and variance (% of score; R2 ) explained by variation of macroscopic evaluation (ME) score for osteophyte
and cartilage lesions and osteophytes only.

TABLE 2. Subchondral Bone Mineral Density (BMD) Measured Using Discussion

Computed Tomography (CT) in Four Compartments
In addition to characterizing equine stifle OA on imaging
Compartments— Mean CT BMD
Depths (mm) (mg/ml, K2 HPO4 ) (±SD) P R2 modalities, this study characterizes a pattern of osteophytes
infrequently described in the literature and specific sites of
LFC—3.75 463.43 (±70.91) P = 0.07 15.0%
LFC—6.25 424.17 (±66.01) P = 0.02∗ 22.9% focal subchondral bone resorption/cyst formation.40 This
LFC—8.75 398.35 (±61.11) P = 0.008∗ 29.2% pattern of osteophytes, presenting as a ridge extending cra-
LTP—5.00 430.59 (±90.23) P = 0.001∗ 40.4%
nially along the MFC to terminate just distal to the MFTR
LTP—7.50 363.35 (±67.95) P = 0.002∗ 38.1%
LTP—10.00 335.78 (±58.56) P = 0.005∗ 32.4% corresponds macroscopically with the MFT joint capsule
MFC—3.75 536.79 (±93.39) P = 0.002∗ 37.8% attachment on the MFC.41 This can be visible on XR, as
MFC—6.25 499.82 (±79.97) P = 0.0009∗ 41.4%
a horizontal mineral opacity line, superimposed with the
MFC—8.75 481.79 (±73.64) P = 0.0006∗ 43.9%
MTP—5.00 301.25 (±70.46) P = 0.03∗ 21.7% MFC (Fig. 5F). Other than anecdotally, this has not been
MTP—7.50 266.59 (±58.16) P = 0.04∗ 19.2% reported.40
MTP—10.00 241.91 (±49.90) P = 0.08 14.2%
As expected, we confirmed that osteophytes are pre-
LFC, lateral femoral condyle; LTP, lateral tibial plateau; MFC, medial dominantly found in the MFT joint, both in terms of
femoral condyle; MTP, medial tibial plateau at three different depths. number of stifles affected and severity of OA lesions.16,21,42
SD, standard deviation; P, P value (∗: significant); R2 , variance of sub-
chondral BMD explained by variation of macroscopic evaluation global
Osteophytes were rarely observed in the femoropatellar
osteoarthritis score. (FP) joint and mostly low grade (1) osteophytes but every
case (n = 13) where one osteophyte was observed in this
CT, presumably within the MFC articular cartilage, and joint also presented osteophytes in the MFT joint. Com-
was thought to represent a central subchondral osteophyte munication between the MFT and FP joints in the horse is
(CO; Fig. 6). variable and reported in as many as 85% of horses, and as
few as 6–19%.22,28,43,44 The two specimens with grade 2 FP
Comparative diagnostic performance of modalities with osteophytes were specimens with the highest ME global
ME OA score. Thereby, we postulate that inflammatory events
Statistically significant linear relationships were found in the femorotibial joints may lead to secondary degenera-
between ME osteophyte global score and CT osteophyte tive changes in the FP joint because of this communication
global score (P ˂ 0.0001), XR osteophyte global score (P = and easy diffusion of inflammatory mediators between
0.005) and US osteophyte global score (P = 0.04; Table 1). compartments. In the same vein, the three specimens with
Statistically significant linear relationships were addition- osteophytes in the lateral femorotibial (LFT) joint with
ally found between ME global OA score and CT osteophyte at least one modality (US, XR, CT) and/or ME, also
global score (P = 0.003) and XR osteophyte global score presented osteophytes in the FP and MFT joints. Com-
(P = 0.01). munication between the FP and LFT joints (3–20%) and
between the MFT and LFT joints (3–5%) is much more
rare.44,45 However, it is reported that in severe OA there can
Computed tomographic subchondral bone density
be a communication between the MFT and LFT joints.8
Lower BMD values were significantly associated with Accordingly, the two specimens with the highest ME global
higher ME global OA score for all four compartments OA score presented osteophytes in both the LFT and
(MFC, LFC, MTP, and LTP) at every depth except at 3.75 MFT joints. Some radiographic projections and CT planes
mm for the LFC and at 10.00 mm for the MTC (Table 2). were particularly useful for the detection of osteophytes
10 DE LASALLE ET AL.
but all projections/planes were needed for a complete
evaluation.
Unsurprisingly, linear relationships between modality
(US, XR, CT) osteophyte global scores and ME osteo-
phyte global scores were stronger than with ME global
OA score that also included cartilage abnormalities. This
discrepancy is explained by the fact that some (eight) speci-
mens presented cartilage lesions without osteophytes. How-
ever, these were only minor cartilage lesions. Although it
has been suggested that osteophytes can develop without
obvious cartilage lesions in equine joints, none of our spec-
imens presented osteophytes without accompanying carti-
lage lesions.46 The strength of the association between ME
osteophyte global scores and imaging osteophyte global
scores was lower than expected (21.9–52.8%; Table 1). This
can probably be explained by differences in appearance
and grading of osteophytes on each modality and at ME.
The strongest linear relationship between CT and ME os-
teophyte global score is likely explained by the advantage
of 3D evaluation with CT, which is closer to ME than
US and XR imaging. The linear relation between US and
both global macroscopic scores (ME osteophyte global
score/ME global OA score) was weaker than for XR and
CT. This can be explained by the fact that the intercondylar
region, which showed an important number of osteophytes,
was not visible with US. In addition, four specimens, includ-
ing one with very high macroscopic scores, were unfortu-
nately not evaluated by US, thereby decreasing the strength
of this analysis.
There was a significant mean difference in osteophyte
global score with XR and CT between observers with one
observer giving systematically higher scores and more so
for CT than for XR. Three-dimensional and multiplanar
reformats evaluations with CT could also have increased
the severity of CT scoring by one evaluator and explained
why the difference was more important with CT. The signif-
icantly higher osteophyte grading of some imaging modal-
ities in comparison to ME may be interpreted in several
ways. Imaging may truly be more sensitive than ME for the
detection of osteophytes, especially CT. Some osteophytes
might be more difficult to detect at ME since they are lo-
cated under the synovial membrane/capsule or ligamen-
tous attachments. Others may be very small or smoothly
surfaced and difficult to differentiate from normal bone.
Conversely, imaging may over interpret normal variations
of articular contour and therefore lack of specificity com-
pared to ME. Normal osseous contour has a particularly
variable appearance at the MFTR, MICE, MTP, and cau-
dal aspect of tibial plateau. The fact that a large number of
grade 1 osteophytes was observed supports that there may
have been overinterpretation of normal osseous contours as
osteophytes. This may also explain the discrepancy between
the screening results and the ME final OA diagnosis. It is
important to remember that screening results were based
2016
on only one radiographic projection and that therefore a
complete radiographic examination could help to detect
normal variations and reduce false positives. In a recent
radiographic study, 84% of actively competing elite show
jumpers presented periarticular new bone formation on the
MTP.18 Perhaps this finding represents, in part, anatomic
variation without clinical significance but this requires fur-
ther study.16,43
In addition to osteophytes, MFC flattening, decreased
joint space width and subchondral sclerosis have been de-
scribed as radiographic signs to evaluate OA, both in gen-
eral and specifically in the stifle joint.6,16,47 Joint space was
not evaluated here since our study was performed ex vivo
and nonweight bearing. Sensitivity, specificity, and inter-
observer agreement of MFC flattening were low enough
to consider that flattening is not an accurate indicator
of macroscopic OA and could be a normal variation of
femoral condylar shape. Finally, subchondral bone sclero-
sis is considered to be of limited discriminatory capacity
in respect to a radiographic diagnosis of OA. Although the
relatively high specificity could indicate that when it is seen,
it is a reasonable indicator of OA, the poor interobserver
agreement negates this limited benefit.
A repeatable pattern of subchondral bone resorption was
observed at the cranial and/or caudal MTP and/or on the
medial aspect of the LFC, in the caudal portion of inter-
condylar fossa. It is interesting to note that some of the
lesions noted with CT on the tibial plateau were visible
retrospectively on radiographs (Fig. 5F). Osseous cyst-like
lesions have been reported on the tibial plateau and LFC
and can be associated with OA.16,42,48 More specifically, a
radiolucent zone in the proximal tibia has been mentioned
in association with degenerative changes of femorotibial
joint secondary to cranial cruciate and/or cranial menis-
cotibial ligament injury.16,48 This is in agreement with what
we observed.
Because of the localization of the bone resorption which
corresponded with apparent vascular channels in OA−
specimens (Fig. 7A, B, E, F), and the absence of those ap-
parent vascular channels, we hypothesized that focal sub-
chondral bone resorption at these sites could represent a
widening of vascular channels leading to subchondral cyst-
like formation. Indeed, prominent widened vascular chan-
nels associated with abnormal bone have been reported on
the medial tibial condyle.49 Because bone resorption was
more prevalent in OA+ specimens (5/7 cystic lesions were
in OA+ specimens), it seems reasonable to assume that
these cyst-like lesions are degenerative and associated to
OA.15,42
COs are commonly present in human knees with OA
and has been reported in the equine metacarpophalangeal
joint and the tarsus and more recently on experimentally
induced OA of the equine stifle.50 In the equine stifle, COs
were described as osseous proliferation adjacent to the
VOL. 00, NO. 0 IMAGING OF EQUINE STIFLE OA
experimental cartilage defect made on the medial trochlear
ridge of the femur to the subchondral bone plate.50
In the only study with a histological evaluation of the
COs, it was described as a projection of dense bone
disrupting the calcified cartilage with overlying cartilage
degeneration.44,46,51–54 In the equine tarsus, COs were only
detected on joints that were OA positives.53,54 Similar
lesions have been described as either hypermineralized
infill phase protrusion or more recently high-density
mineralized protrusions (HDMP) in the equine fetlock,
tarsus, and carpus.53–56 The relationship between HDMPs
protruding into cartilage at the ultrastructural level and
COs observed with clinical imaging is currently unknown
and requires further investigation.56
Since alterations of subchondral BMD sporadically oc-
cur in conjunction with OA, a major advantage of CT was
the measurement of BMD.30,32 Noninvasive bone-mineral
analysis with CT has been used in horses to study bone den-
sity but never in the stifle.30,31 Contrary to our expectations,
a significant decrease in BMD was observed with increased
severity of OA. Also, the mean CT-BMD obtained for the
MFC was lower (506 mg/ml) than the mean DEXA-BMD
(0.78 ± 0.16 g/cm3 = 780 ± 16 mg/ml) obtained in a
previous study on eight healthy horses.32 Our findings are
contrary to results on osteoarthritic metacarpophalangeal
joints of racehorses, but consistent with results reported in
many animal models of early OA including a rabbit model
of acutely-induced stifle OA.30,33,57–65 Those models sug-
gest that resorption of the subchondral bone may be a part
of OA pathogenesis. Because OA was likely chronic in our
study, a mismatch in bone resorption/formation could re-
sult from a chronic reduction of joint load secondary to
reduced usage, weight loss, and aging. Indeed, in humans,
a decrease in BMD is reported in severe chronic femorotib-
ial OA.66,67 Although our observations were contrary to
our expectations, it would be interesting to repeat measure-
ments in a larger clinical study and relate them to age and
activity.
It is important to remember that OA is a disease involv-
ing all joint tissues including articular cartilage, subchon-
dral bone, synovial membrane, joint capsule, joint fluid,
and menisci.20 Unfortunately, most of the joint in the study
herein were collected from the abattoir and assessment of
all the soft tissues was not possible. Since, cartilage eval-
uation is not possible with XR and CT (without arthrog-
raphy) and limited to some areas with US, cartilage le-
sions were only evaluated macroscopically in our study.
CT-arthrography has been described in horses for soft tis-
sue and cartilage evaluation.28,29 However, as this study
was ex vivo, we thought some specimens might have ar-
ticular capsule laceration, which would make arthrography
impossible. Another limitation of our ex vivo study is that
the clinical significance of lesions could not be determined.
Also, some sites were not visible with US and ME. Indeed,
only a portion of the intercondylar region is visible with US
11
and requires flexion of the stifle, which was not always pos-
sible ex vivo.21,68 Also, ME of femoral epicondyles and cra-
nial tibia was limited by soft tissue attachments and those
sites were not included here. Only one evaluator performed
US and interobserver variation could not be calculated.
Also, intraobserver variation was not evaluated in this
study.
In conclusion, this study is the first that describes specific
OA lesions in the equine stifle using US, XR, CT, and
ME. For stifles included in this sample, osteophytes were
predominantly found in the MFT joint and exhibited a spe-
cific pattern associated with the insertion of the MFT joint
capsule cranially on the MFC. Imaging may be more sensi-
tive than ME in detection of some osteophytes but readers
should be cautioned against over interpreting normal
anatomic variations as osteophytes. Computed tomogra-
phy examination revealed COs and subchondral bones
changes. Naturally acquired equine stifle OA was associ-
ated with a decrease in BMD. Specific sites of subchondral
bone resorption were apparent with CT and may represent
widened vascular channels and/or enthesopathies on cru-
ciate and/or meniscotibial ligament insertions. In the near
future many equine imaging centers will be able to offer CT
and MRI examinations of the equine stifle.23,25,69 However,
US equipment is available to most equine practitioners
and the study herein confirms that it is complementary to
a radiographic examination. This is particularly valuable,
as the radiographic parameters of flattening and sclerosis
of the MFC do not appear to be reliable indicators of
equine stifle OA. Further studies in vivo are needed
in order to better understand the clinical significance
on OA lesions observed on various diagnostic imaging
modalities. A better knowledge and identification of
pathology will allow us to detect equine stifle OA earlier
and may allow us to intervene therapeutically before
advanced structural changes and thereby improve the
long-term prognosis.
LIST OF AUTHOR CONTRIBUTIONS
Category 1
(a) Conception and Design: Julie De Lasalle, Kate Alexander, Sheila
Laverty
(b) Acquisition of Data: Julie De Lasalle, Kate Alexander, Sheila
Laverty, Julien Olive
(a) Analysis and Interpretation of Data: Julie De Lasalle, Kate
Alexander, Sheila Laverty
Category 2
(a) Drafting the Article: Julie De Lasalle
(b) Revising Article for Intellectual Content: Kate Alexander, Sheila
Laverty, Julien Olive
Category 3
(a) Final Approval of the Completed Article: Julie De Lasalle, Kate
Alexander, Sheila Laverty, Julien Olive
12 DE LASALLE ET AL. 2016

ACKNOWLEDGMENTS Lachance for technical assistance in imaging procedures; France God-

The authors thank Hélène Richard for laboratory support; Gabrielle bout and Nicolas Anne-Archard for image conception; Huguette
Martel for assistance with specimen dissection; Cynthia Lapierre, Mallet for bibliography; and Guy Beauchamp, PhD, for statistical
Anne-Marie Martel, Christine Chevrier, Geneviève Rouleau, and Suzie analysis.

APPENDIX 1. Abbreviations for Terms Used in This Study

Abbreviation Term Abbreviation Term

BMD Bone mineral density LTP Lateral tibial plateau
Ca60L-CrMO Caudo-60°lateral-craniomedial oblique ME Macroscopic evaluation
Ca60M-CrLO Caudo-60°medial-craniolateral oblique MFC Medial femoral condyle
Ca10Pr5L-CrDiMO Caudo-10°proximo-5°lateral-cranio-disto-medial oblique MFE Medial femoral epicondyle
COs Central subchondral osteophytes MFT Medial femorotibial
CrT Cranial part of tibia MFTR Medial femoral trochlear ridge
CT Computed tomography MICE Medial intercondylar eminence
DEXA Dual-energy X-ray absorptiometry MP Medial part of patella
DP Distal part of patella MTP Medial tibial plateau
FP Femoropatellar OA Osteoarthritis
ICF Intercondylar fossa of femur OCD Osteochondritis dissecans
LFC Lateral femoral condyle PP Proximal part of patella
LFE Lateral femoral epicondyle
LFT Lateral femorotibial ROI Region of interest
LFTR Lateral femoral trochlear ridge US Ultrasonography
LICE Lateral intercondylar eminence XR Computed radiography
LM Lateromedial

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