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The Veterinary Journal 191 (2012) 193–198

Contents lists available at ScienceDirect

The Veterinary Journal


journal homepage: www.elsevier.com/locate/tvjl

Ultrasonographic evaluation of the coxofemoral joint region in young foals


U. Rottensteiner a, F. Palm b, J. Kofler a,⇑
a
Department of Large Animal Surgery and Orthopedics, Equine Clinic, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria
b
Department of Gynecology, Andrology, Obstetrics and Embryonic Transfer, Equine Clinic, University of Veterinary Medicine Vienna, Veterinaerplatz 1, 1210 Vienna, Austria

a r t i c l e i n f o a b s t r a c t

Article history: The purpose of this study was to map the coxofemoral region in foals to obtain ultrasonographic refer-
Accepted 8 February 2011 ence values for the interpretation of potentially pathological findings in hip joints. Using a 7.5 MHz linear
transducer, 38 examinations were carried out: 10 (20 joints) on cadavers and 28 (55 joints) on live
healthy foals up to 8 weeks of age. The chosen plane of examination was caudolateral–craniomedial obli-
Keywords: que on an imaginary line connecting the greater trochanter and the cranial edge of the tuber sacrale.
Ultrasonography The relatively thin muscular layer covering the coxofemoral joint allowed good image quality. The
Coxofemoral joint
evaluated structures included the bone surface of the ilium and acetabulum, the subchondral bone on
Foal
Septic arthritis
the femoral head and greater trochanter, the joint cartilage on the femoral head, the fibrocartilaginous
acetabular labrum, the femoral capital physis, the cartilaginous layer covering the greater trochanter,
the joint capsule and the presence of visible synovial fluid and the gluteal muscles. A bilateral anatomical
frozen section in the plane of examination was made in one cadaver. A good correlation was found
between ultrasonographic and corresponding anatomical measurements on the frozen section. This study
indicated that ultrasound is a valuable diagnostic tool which can provide good image quality in neonates.
Ó 2011 Elsevier Ltd. All rights reserved.

Introduction the exact origin requires experience in interpretation and special


equipment (Steckel, 1991), which is usually only accessible in large
Diseases of the coxofemoral joint are a relatively uncommon clinics. Furthermore, young growing animals retain an increased
cause of lameness in horses (Dyson, 2003). However, the predispo- amount of radioactive marker in physes and epiphyses of long bones
sition of young horses for diseases, such as fractures of the femoral (Metcalf et al., 1989), which makes scintigraphic examination diffi-
neck (Hunt et al., 1990) or the acetabulum (Hendrickson, 2002b), cult in foals. Thermography can rarely determine the exact cause of
haematogenous septic arthritis (McIlwraith, 2002) or luxation of an inflammatory process (Turner, 1991) but ultrasonography is a
the coxofemoral joint (Malark et al., 1992), underlines the neces- relatively cheap, non-invasive method that is accessible to most
sity of a detailed investigation of this region in lame foals. equine practitioners. Transcutaneous and transrectal scanning
In addition to a thorough clinical examination and intra- techniques have been described in horses (Tomlinson et al., 2001;
articular analgesia (Stashak, 2002; Bassage and Ross, 2003; Kofler, Brenner and Whitcomb, 2007, 2009) as well as in other species
2009a,b), different methods of diagnostic imaging are applied to (Kresken, 2001; Grubelnik et al., 2002) but to the best of our knowl-
evaluate the coxofemoral region in horses. Radiography is nor- edge, a thorough ultrasonographic examination of the coxofemoral
mally recommended to diagnose fractures of the femoral capital joint in foals has not been reported.
physis or the acetabulum and luxations of the hip joint (Hunt This study was performed to gain an overview of the normal
et al., 1990; Hendrickson, 2002a,b; Sullins, 2002). This usually re- sonoanatomy of the coxofemoral joint in newborn foals, as well
quires dorsal recumbency, which can only be achieved with gen- as to obtain reference values for the anatomical structures in this
eral anaesthesia in adult horses. In foals, deep sedation often region. Since the growth of foals takes place mainly in the first
provides a sufficient relaxation of muscles. However, a pre-existing months of life, with light breeds reaching about 30% of their moth-
injury of the hip joint can be further impaired during induction and ers’ bodyweight (BW) at the age of 3 months (Hois et al., 2005), we
recovery (Pilsworth, 2003). Standing radiography yields reliable re- hypothesised that structures would grow in correlation to age and
sults (Geburek et al., 2009), but exposes personnel to a radiation body mass of the foals.
hazard (Pilsworth, 2003).
Scintigraphy is a relatively new diagnostic tool. It offers high sen- Materials and methods
sitivity, but low specificity compared to radiography. Determining
Animals

⇑ Corresponding author. Tel.: +43 1 25077 5511. Foal cadavers and live neonates up to 8 weeks of age that had been hospitalised
E-mail address: Johann.Kofler@vetmeduni.ac.at (J. Kofler). at the University of Veterinary Medicine Vienna and treated or euthanased for

1090-0233/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.tvjl.2011.02.012
194 U. Rottensteiner et al. / The Veterinary Journal 191 (2012) 193–198

reasons other than hindlimb lameness were examined. If foals had been hospita- Frozen sections
lised for a longer period, a follow-up examination was carried out after at least
5 days. With each live foal, the owner’s consent was requested prior to examination. Following ultrasonography, both hip joints of one cadaver were frozen for
All procedures were approved by the Institutional Ethics and Animal Care Com- 3 weeks in a position similar to standing horses and sectioned with a band saw
mission of the University of Veterinary Medicine Vienna. in the plane of the examination. Anatomical measurements were taken as for ultra-
sonography and compared to respective data.
Exclusion of lameness
Statistical analysis
A short lameness evaluation, consisting of palpation of the coxofemoral region
and inspection while standing, walking and possibly trotting, was performed in Statistical analyses were carried out in collaboration with the Platform Biosta-
every foal (Kofler, 2009a). In cadavers, recent hindlimb lameness was excluded by tistics of the University of Veterinary Medicine Vienna (Dr. A. Tichy) using SPSS 17.
reviewing the history of the animal and the observed dissection findings following For all measurements, a mean, standard deviation (SD) and range of values were
ultrasonographic examination (i.e. gross appearance of the joint cartilage, joint cap- calculated. A correlation between age/body mass of the foals and the obtained mea-
sule and synovial fluid). surements was evaluated using Pearson’s correlation. The assumption of normal
distribution was proved using the Kolmogorov–Smirnov test. To test for differences
between sides of the pelvis, a paired samples t test was applied. Multiple measure-
Ultrasonographic examination technique
ments of the same animal were aggregated to a single value. For all tests, signifi-
cance was set at P 6 0.05, and P 6 0.001 was defined as highly significant.
Ultrasonography was performed in stalls with the mare present. Foals were re-
strained in the standing position by firmly holding the tail and thorax. No sedation
was given. The area between the tuber coxae and the greater trochanter was moist-
Results
ened with alcohol, and acoustic coupling gel was applied; the coat was not clipped
in living foals. During examination, care was taken that foals were bearing weight
on both hindlimbs. Thirty-eight examinations (including follow-up examinations)
Cadavers were stored in a cooling chamber at +4 °C and examined within 24 h in 27 different foals were carried out. Twenty-eight examinations
of euthanasia. The body was placed in lateral recumbency and the legs were angled were performed on living foals and 10 on cadavers. The foal ages
similar to the position in standing foals. The area between the tuber coxae and the
greater trochanter was clipped before applying alcohol and coupling gel.
ranged from 0 to 56 days (mean 13.9 days, SD 16.2), BW mass ran-
For all foals, a 7.5 MHz linear probe without a stand-off pad was used (Sonoline ged from 39 to 140 kg (mean 81.9 kg, SD 29.0). Sex, breed and rea-
Sienna, Siemens). The probe was positioned in a caudolateral–craniomedial oblique son for hospitalisation or euthanasia are summarised in Table 1.
plane (from the greater trochanter to the cranial edge of the tuber sacrale; Fig. 1), The history of the foals did not reveal any hindlimb lameness in
according to a similar study in newborn calves (Grubelnik et al., 2002); this plane
the days immediately prior to ultrasonographic evaluation. At
provided an excellent longitudinal overview of the structures in this region. Both
hip joints were evaluated. All evaluations were performed by the first author (UR). lameness examination, none of the foals showed obvious hindlimb
lameness or any other abnormality of the coxofemoral region. A
Evaluated structures small number of foals could be evaluated only at the walk due to
handling difficulties when trotting. One foal (No. 13) was in lateral
The following anatomical structures were examined and the indicated parame- recumbency due to tendon contracture in both forelimbs; in this
ters were evaluated: neonate, examination included inspection and palpation of both
(1) Pelvis: echogenicity and surface of the acetabulum and the body of the
hip joints as well as passive flexion, extension and rotation; no
ilium; echogenicity and structure of the acetabular labrum; abnormality was detected.
(2) Femur: echogenicity, structure, surface and subchondral bone surface of the The time required for a full ultrasonographic examination of the
joint cartilage on the femoral head and neck, the cartilaginous femoral cap- hip joint varied greatly depending on the temperament of the foals
ital physis and the cartilaginous layer on the greater trochanter;
and the resulting image quality; in calm foals with a good image
(3) Soft tissues: echogenicity and structure of the joint capsule and the gluteal
muscles covering the coxofemoral joint; presence of visible joint fluid quality, it was approximately 5–10 min for each joint. In four foals,
between joint cartilage and capsule. image quality was poor due to handling difficulties; these foals
were excluded from this study. In one case, only unilateral exami-
Seven parameters were measured in each joint (see Fig. 2). All images were nation was possible for the same reason (foal No. 7). Image quality
printed out and/or stored as a digital version. Prior to statistical analysis, all data was excellent in all cadavers and good to excellent in most stand-
including history and all measurements were reviewed; the quality of the images
was graded subjectively (excellent, good, acceptable, poor). Measurements that ap-
ing foals; however, in some large foals the 7.5 MHz probe yielded
peared imprecise on the print-out were excluded from the study. only acceptable results (foal No. 4, 5, 7, 9, 12 and 18). The coxofem-
oral joint of breeds with very thick coat (Haflinger, foal No. 9) was
difficult to examine without clipping.

Pelvis

The lateral bony surface of the ilium and acetabulum appeared


as a hyperechoic, smooth line. The cartilaginous acetabular labrum
could be imaged in all foals as a hypoechoic, homogenous or
slightly heterogenous, triangular structure attached to the margin
of the bony acetabulum. The length ranged from 6.0 to 14.9 mm
(mean 9.28 mm, SD 1.76). There was a statistically significant cor-
relation between the length of the acetabular labrum and age
(P < 0.001), and the body mass (P < 0.05) of the foals.

Femur

The joint cartilage appeared as a hypoechoic, homogenous band


with a smooth surface covering the bony contour of the femoral
head and neck. In some joints, small echoic spots were imaged
Fig. 1. Examination plane. The probe was positioned in a craniomedial-caudolateral within the cartilage. The subchondral bone surface appeared
oblique plane (S1: cranial edge of the tuber sacrale; GT: greater trochanter). slightly irregular in some cases (Fig. 3).
U. Rottensteiner et al. / The Veterinary Journal 191 (2012) 193–198 195

Fig. 2. Measurements carried out in each joint: (1) Distance between skin surface and the bony edge of the acetabulum; (2) Length (cranial-caudal) of the acetabular labrum;
(3) Thickness of the joint capsule at its origin at the acetabular labrum; (4) Thickness of the joint cartilage of the femoral head just caudal to the end of the acetabular labrum;
(5) Thickness of the joint capsule measured halfway between its origin and the capital femoral physis; (6) Thickness of the joint cartilage just cranial to the capital femoral
physis; (7) Thickness of the cartilaginous layer on the greater trochanter at its thickest point. AC, acetabulum; FH, femoral head; PH, capital femoral physis; GM, gluteal
muscles; GT, greater trochanter. Left, craniomedial; right, caudolateral.

Table 1
Animal data of the 27 examined foals.

Sex Breed Living foal/ Reason for Reason for euthanasia Follow-up examination
cadaver hospitalisation
1 M TB Living Surveillance
2 F TB Living Surveillance
3 M Pinto Living Prematurity Two follow-up examinations
4 F WB Living Septicaemia
5 M Trakehner Living Insemination mare Two follow-up examinations
6 M WB Living Insemination mare
7 F WB Living Insemination mare One follow-up examination with only unilateral examination due to
handling difficulties
8 M SB Living Surveillance, Three follow-up examinations
insemination mare
9 M Haflinger Living Colic
10 F WB x Living Septicaemia
Haflinger
11 F Lipizzaner Living Failure of passive
transfer
12 F WB Living Insemination mare
13 M SB Living + cadaver Tendon contracture Tendon contracture One follow-up examination after euthanasia
forelimbs forelimbs
14 M WB Living Respiratory disease
15 M WB Living Septicaemia
16 M WB Living Persistent rachis One follow-up examination
17 F TB Living Surveillance One follow-up examination
18 M SB Living Abscess larynx
19 M Trakehner Cadaver Caesarean, born dead
20 F WB Cadaver Septicaemia
21 F Trakehner Cadaver Septicaemia
22 M WB Cadaver Umbilical hernia
23 F WB Cadaver Septicaemia
24 F SB Cadaver Meconium blockage
25 M SB Cadaver Prematurity
26 M SB Cadaver Prematurity
27 F WB Cadaver Atresia coli

M, male; F, female; TB, Thoroughbred; SB, Standardbred; WB, Warmblood; Surveillance, surveillance of parturition and pregnancy.

The thickness of the joint cartilage just caudal to the acetabular neck. The bone under the cartilage appeared smooth and regular
labrum ranged from 1.7 to 5.7 mm (mean 2.73 mm, SD 0.83) and in all but two cases (foal Nos. 24 and 26). In larger foals, imaging
from 3.8 to 8.0 mm next to the femoral capital physis (mean the physis was difficult, because heavy musculature impeded us
5.41 mm, SD 0.86). There was no statistically significant correlation from positioning the probe at the right angle (beam directed slightly
between age or BW and joint cartilage thickness. caudal) to visualize the physis covered by the greater trochanter.
The cartilaginous femoral capital physis was imaged as a homo- The cartilaginous layer on the greater trochanter appeared as a
genous, hypo- to anechoic gap in the bony surface of the femoral hypoechoic semilunar structure with a smooth surface and echoic
196 U. Rottensteiner et al. / The Veterinary Journal 191 (2012) 193–198

mass (P < 0.05), and a low correlation (P = 0.044 left/0.067 right)


between this parameter and the age of the foals.

Soft tissues

The joint capsule was imaged as an echoic, homogenous band


overlying the hypoechoic homogenous joint cartilage. Thickness
at its origin at the acetabular labrum was 2.8–5.5 mm (mean
3.99 mm, SD 0.50). Between the acetabular labrum and the femoral
capital physis, the thickness of the joint capsule ranged from 0.5 to
2.0 mm (mean 0.82 mm, SD 0.25). There was no statistically
significant correlation between age/body mass and thickness of
the joint capsule.
In all standing foals, the joint capsule was taut and close to the
joint cartilage. In 6/11 foals in lateral recumbency, however, there
was a thin (mean 0.51 mm, SD 0.23) anechoic band overlying the
joint cartilage consistent with synovial fluid (Fig. 5).
The gluteal musculature appeared hypoechoic with distinct
echoic lines, consistent with strong connective tissue. The distance
between the skin surface and the edge of the acetabulum was
highly variable and ranged from 19.6 to 69.9 mm (mean
40.13 mm, SD 11.81). There was a strong correlation between this
distance and age/BW (P < 0.001).
There was no statistically significant difference between left
and right sided structures. No cadaver joint showed any signs of
disease at dissection: the joint cartilage appeared white and
smooth, the joint capsule was thin and the synovial fluid was
Fig. 3. Slightly irregular subchondral bone surface at the femoral head (arrows). JC, physiological concerning amount and quality.
joint cartilage; FH, femoral head; GM, gluteal muscles. Left, craniomedial; right,
caudolateral.
Frozen sections

All structures evaluated ultrasonographically were also visible


spots. The subchondral bone surface appeared highly irregular in
on frozen sections. All except two measurements taken from the
many cases (Fig. 4). The thickness of this structure was highly var-
frozen sections were similar to data from ultrasonography. The dis-
iable and ranged from 5.8 to 16.0 mm (mean 10.08 mm, SD 2.12).
tance between skin surface and the edge of the acetabulum ap-
There was a statistically significant correlation between the thick-
peared larger on frozen sections (46.0/49.0 mm) than the
ness of the cartilaginous layer on the greater trochanter and body
respective data on ultrasound (29.1/32.2 mm). The cartilaginous
layer on the greater trochanter appeared thicker on frozen sections
(16.0/15.0 mm) than on ultrasonography (12.2/11.5 mm).

Fig. 5. Thin anechoic band overlying the joint cartilage, consistent with synovial
Fig. 4. Highly irregular subchondral bone surface at the greater trochanter (arrow). fluid, imaged in some recumbent foals. AC, acetabulum; LA, acetabular labrum; FH,
GT, greater trochanter. Left, craniomedial; right, caudolateral. femoral head; GM, gluteal muscles. Left, craniomedial; right, caudolateral.
U. Rottensteiner et al. / The Veterinary Journal 191 (2012) 193–198 197

Discussion The greater extent of this structure could be explained by an


incomplete ossification process of the apophysis at the greater
This study aimed to image the structures of the coxofemoral trochanter. Small echoic spots within the cartilage could represent
joint region in newborn foals up to an age of 8 weeks. As found fibres of the matrix or focal ossification (Denoix, 1996).
in a similar study on newborn calves (Grubelnik et al., 2002), the The fibrocartilaginous acetabular labrum was imaged as a
7.5 MHz linear probe yielded a good image quality and an excellent hypoechoic, homogenous or slightly heterogenous triangular
overview of the anatomical structures in this region. Clipping was structure at the edge of the acetabulum, which is similar to find-
not necessary in small foals but in larger foals image quality was ings in newborn calves (Grubelnik et al., 2002). In adult horses,
impaired by a lack of acoustic coupling due to dense coat. Thus, the labrum has been described in anatomical literature (Zietzsch-
we highly recommend clipping when detailed imaging is required mann et al., 1977; Nickel et al., 2001a,b; Kainer, 2002), but cannot
for an accurate diagnosis. be imaged ultrasonographically because of a lower resolution due
Foals were not sedated for the examination in this study. In to the heavy muscles covering the coxofemoral joint (David et al.,
most cases foals could be restrained sufficiently well to gain good 2007).
or excellent data. However, image quality was impaired in some The femoral physis was clearly visible as an anechoic gap in the
cases and foals should be sedated if a more precise diagnosis is bony contour of the femoral neck and must not be misinterpreted
required. as a fracture line. A physeal fracture characteristically produces a
As in similar studies in adult horses (Tomlinson et al., 2001), the proximal dislocation of the greater trochanter and therefore a step
differences between structures measured on each side of the pelvis is seen in the bony surface (Craychee, 1995; Geburek et al., 2009).
were not significant. However, measurements of the distance be- Osteomyelitis of this area, as with neonatal sepsis, produces an
tween skin and acetabulum were different in some individuals. A irregular bone echo together with fluid accumulation in the sur-
reason for this could be a variable compression of the gluteal mus- rounding soft tissues (Craychee, 1995; Denoix, 1996).
cle due to the necessary pressure exerted by the probe (Denoix, In this study there was a highly significant correlation between
1996). Similarly, muscle compression could have caused a smaller age/BW of the foals and the distance between skin and acetabu-
distance between skin and acetabulum on the ultrasonographic lum. This measurement was not performed in adult horses (Toml-
image when compared to the measurement on the frozen sections. inson et al., 2001), but could be of major interest when
Care should therefore be taken to keep pressure equal in this re- arthrocentesis is planned. However it is important to be aware that
gion when ultrasonic examination of clinical cases is performed. the distance is highly dependent on the pressure exerted by the
In newborn foals, the greater trochanter is a very prominent probe.
protuberance due to weak surrounding muscles. At the cartilagi-
nous layer on the greater trochanter, we observed a similar differ- Conclusions
ence in measurements between left and right as well as between
ultrasonography and frozen sections in some cases. We therefore This study showed that ultrasonography produced reliable
assumed that the different measurements were due to the probe images of the structures of the coxofemoral region in young
sliding over this prominence, leading to a slightly different exam- foals, and the physiological fluid volume within the joint could
ination plane. Another explanation could be differences in ossifica- not be imaged. Ultrasound has been shown to be a valuable
tion of the apophysis of the greater trochanter. diagnostic tool which provides good image quality in neonates.
The joint cartilage of the femoral head appeared as a homoge- Further studies should compare the present data to images ob-
nous, hypoechoic band with some echoic spots and a smooth sur- tained from diseased hip joints and investigate the sensitivity
face, similar to the appearance in newborn calves (Grubelnik et al., and specificity of ultrasound in the detection of various patho-
2002). Contrary to this, in adult horses the thin joint cartilage ap- logical conditions.
pears as a completely anechoic or very poorly echoic rim (Denoix,
1996), similar to adult cattle (Grubelnik et al., 2002). The thickness
and echogenity of the joint cartilage in equine neonates should not Conflict of interest statement
be misinterpreted as an inflammatory exudate, such as in joints
showing septic arthritis which can produce similar ultrasono- None of the authors has any financial or personal relationships
graphic findings (Kofler, 2009c). Criteria for septic inflammation with other people or organisations that could inappropriately
of the joint could be echoic particles (e.g., fibrin clots) adhering influence or bias the content of the paper.
either to the cartilage surface or the synovial membrane, increased
echogenicity of the synovial fluid, echoic particles within the joint Acknowledgements
cavity, thickening of the synovial membrane, distension of the joint
capsule and flow-phenomena (Denoix, 1996; Kofler, 2009c). The author would like to thank Dr. Alexander Tichy (Institute
The subchondral bone surface appeared irregular in some joints for Medical Physics and Biostatistics, University of Veterinary Med-
in this study. In adult horses, every irregularity of the bony contour icine Vienna) for the statistical analyses.
of the femoral head should be considered as a pathological condi-
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