The site of focal osteomyelitis lesions in foals
E. C. Firth' and S. A. Goedegebuure2
SUMMARY The long bone ends of foals with infectious disease were sawn into sagittal slabs,
washed and inspected. Tissue suspected to be abnormal on the basis of change of colour and
consistency was radiographed, and then decalcified and examined histologically. The exact site
of 140 focal osteomyelitis lesions from 18 foals was determined. There were more lesions in the
epiphysis than the metaphysis. Epiphyseal lesions were in specific sites within a given epiphysis,
and in most epiphyses the lesions were at the site of thickest cartilage. Metaphyseal lesions in
the metacarpal, metatarsal and distal radial growth plates tended to be on the more inclined
parts of the growth plate.
INTRODUCTION
Infectious arthritis is a serious disease of young foals and most cases are
complicated by the concurrent presence of osteomyelitis in the bone adjacent to the
affected joint. In one study, about 70% of foals presented for examination of joint
ill had osteomyelitis in one or more bones (2). The most commonly affected sites
have been described in radiographic and pathological studies (1, 4, 5).
No reason for the apparent predisposition of some bone ends to osteomyelitis has
so far been given, and the suggestion that infection occurs more often in one
particular site than another within a given bone end has not been put forward. One
of us noted that epiphyseal osteomyelitis often occurred at or near the site of the
thickest 'articular' cartilage in a particular bone end. The sites of thick cartilage in
the major joints of the foal has recently been described (3). In this paper we describe
the sites of focal osteomyelitis lesions in young foals with naturally occurring
haematogenous arthritis/osteomyelitis.
MATERIALS AND METHODS
The bones of 18 foals aged 4-150 days old were obtained from routine post-mortem material.
The cause of death or euthenasia is shown (Table 1). All foals included had a history of
predisposition to infection (early birth, late standing or sucking after birth, perinatal
disease, etc), had evidence of infectious disease prior to death or at necropsy, and had bone
lesions in more than one limb.
The limbs were boned out, and the ends of the long bones were sawn off about 5 cm from the
metaphyseal growth plate, so that metaphysis, physis, epiphysis and articular cartilage
could be examined. The following bones were collected: proximal and distal humerus,
proximal and distal radius, distal third metacarpal bone, proximal and distal femur,
proximal and distal tibia, talus, and distal third metatarsal bone. The bones were sawn into
sagittal slabs 4-7 mm thick with a bandsaw, washed in running water, and examined visually
under bright light, in most cases before fixation in 4% buffered formalin. Each slab was
numbered. The slabs were radiographed in a Faxitron 43805N X-ray apparatus (HewlettPackard, McMinnville, CA, USA) and the films were hand developed.
The visual and radiographic examinations were performed to determine the presence and
site of focal lesions. Defects which were so extensive that the whole epiphysis or metaphysis
was destroyed, making it impossible to pinpoint the site at which the process had begun,
were discarded from the study. Localised lesions (i.e. less than 10 mm diameter) were
detected by observing round or irregularly shaped discoloration (whitening) of the
cancellous bone or absence of bone and/or cartilage with replacement by exudate or soft
necrotic tissue.
1
2
Dept of Large Animal and General Surgery, State University Utrecht, P.O. Box 80.153, 3508 TD
Utrecht, The Netherlands. Present address: Massey University, Palmerston North, New Zealand.
Dept of Veterinary Pathology, State University Utrecht, P.O. Box 80.158, 3508 TD Utrecht, The
Netherlands.
THE VETERINARY QUARTERLY, VOL. 10, No. 2, APRIL 1988
99
Table I. Cause of death or reason for euthanasia of 18 foals with focal osteomyelitis. All bacteriological determinations were conducted on material collected at necropsy, except those mentioned under
'joints', synovia from which was collected by sterile arthrocentesis at the time of clinical examination.
Bone culture at necropsy implies sampling of macroscopically visible lesions.
*Synovia was repeatedly negative at the time of distal radial osteomyelitis, 5 months before euthanasia.
TT=tibio-tarsal, BHS=beta haemolytic streptococcus, DJD=degenerative joint disease, MtPJ=metatarsophalangeal joint, Mt3=third metatarsal bone, WPN=Dutch Warmblood.
Foal
Breed
8401
WPN
10
8410
WPN
4
8411
WPN
8412
Age
days
Other Necropsy Lesions
Culture
metaphysitis,
path. fracture Mt3
Proteus fracture
site
polyserositis, meningitis
polyarthritis, omphalitis
E.coli
bones/organs
11
polyarthritis
E.coli T-T joint
12
omphalitis, polyarthritis
culture negative
28
osteomyelitis tibia
E.coli distal tibia
8419
mini Shet
8507
WPN
10
polyserositis
E.coli organs
8512
WPN
14.
polyarthritis
E.coli 2 joints
8521
WPN
30
bronchopneumonia osteomyelitis L&R dist, femurs
and R ulna
BHS lung, C.equi
lung abscess
8602
WPN
24
bronchopneumonia polyosteomyelitis
E.coli 4 joints
8603
WPN
21
polyosteomyelitis
E.coli 2 joints;
several bones
8309
WPN
omphalophlebitis,
persistent urachus,
polyarthritis, rib
osteomyelitis
BHS navel, E.coli
femur, ulna, rib
793
WPN
11
omphalitis, bronchopneumonia, polyosteomyelitis
E.coli
bones/organs
8004
WPN
28
osteomyelitis proximal ,
humerus
not done
8037
WPN
150
DJD radiocarpal joint
synovia negative*
8119
pony
polyarthritis
not done
8123
WPN
120
physitis Mt3, arthritis
MtPJ
synovia culture
negative
8127
WPN
13
polyarthritis/osteomyelitis
omphalophlebitis, endocarditis
Klebsiella bones
8510
WPN
polyosteomyelitis
not done
100
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10, No. 2, APRIL 1988
Suspected changes were recorded by photography, usually of the whole series of slabs of the
bone end concerned, in order to show the exact site of the lesion. In some cases, photography
of (part of) an individual slab was used to record the nature and form of the lesion. On the
radiographs, the presence of localised lesions was suggested by focal osteolysis.
When visual and/or radiographic evaluation indicated that lesions were present, or might be
present, the part concerned was decalcified in 35% formic acid and 6.8% sodium formate,
rinsed in running water, and embedded in paraffin. Sections were cut at 6u and stained with
haematoxylin and eosin (HE) and Azan.
In this group of young foals, the diagnosis of osteomyelitis was based on the presence of
history typical of bone infection (2), the multifocal nature of the disease, evidence of other
infectious disease in other organs at necropsy, and histological findings in bone and carti-
lage. In some cases clinical and laboratory findings were also contributory. Culture of
synovial fluid taken at clinical examination was positive in 3 foals. In 6 foals, bacteriological
culture of suspected abnormal bone was performed after sawing of the bone end, flaming the
lesion, and inserting the swab deep into the bone lesion. Laboratory culture techniques have
been previously described (2). For inclusion in this study, the histological criteria consistent
with osteomyelitis included one or more of: exudate in marrow spaces and vessels with
polymorphonuclear or mononuclear cellular infiltration, thrombosis of vessels, necrosis of
marrow tissue or bone or cartilage, and absence of bone or cartilage and replacement by
exudate, necrotic debri, or fibrosis.
RESULTS
Of a total of 35 sets of limbs sawn and examined, those of 18 foals were included in
the study. The others were rejected because no lesions were found on macroscopic
or radiological examination, or because the nature of the lesions did not support
the diagnosis of active or chronic bone infection. E.coli was by far the most
commonly isolated micro-organism (Table 1).
In almost all cases, the focal lesions were detected by visual examination, because
discoloration or bone loss was visible on one or both surfaces of one or more slabs.
The discoloration was white or yellow, and it surrounded areas of focal bone loss,
which was evidenced by a small or large cavity filled with glistening exudate or dull
necrotic material. The lesions were all at the junction of bone and cartilage, and
occurred at, or very close to, the junction of epiphyseal bone and the cartilage
covering the articular aspect of the epiphysis, or at the junction of bone and physeal
cartilage, usually on the metaphyseal side of the growth plate. These lesions have
previously been referred to as E or P lesions respectively (2).
Extension of the lesion into epiphyseal bone was evident in some cases, and in
others there was extension into the deeper layers of cartilage. In some instances
there was penetration of the articular surface by the infectious process. Almost all
lesions near the metaphyseal growth plate showed cartilage destruction and either
radiological and/or histological evidence of involvement of bone on the opposite
side of the growth plate. The presence of the lesions was confirmed by histological
study, and the extent of the lesions was often better demonstrated by radiology.
Usually, the extent of bone loss evident on radiological and/or histological exam-
inations indicated the probable site of origin of lesions near the metaphyseal
growth plate.
The incidence of lesions in the various foals, and a breakdown of the number of
lesions in each bone end, are shown in Table 2 and Fig. 1 respectively. The sites of
the focal osteomyelitis lesions in each bone end were as follows.
Proximal humerus. There were 6 lesions in the caudo-central aspect of the
epiphysis. In some cases the lesion extended through up to 4 slabs. The apparent
site of origin of the process was not constant, being the epiphysis in 4 cases and the
metaphysis in 2 cases, and the lesion extended through the growth plate. There was
one metaphyseal lesion found at the proximal humeral growth plate ventral to the
major tubercle.
THE VETERINARY QUARTERLY, VOL. 10, No. 2, APRIL 1988
101
Table 2. Site of lesions found in long bone ends of 18 foals. The first number identifies the foal,
R=right, L=left; the last digit(s) indicate the slab(s) involved. E=epiphyseal osteomyelitis, P=osteomyelitis at the physis. a=radiographically or histologically detected bone lysis. MtHI=third metatarsal
bone, McIII=third metacarpal bone, T=trochanter, U=ulna.
8412L 3
L 6
R5-7
R 4
P
P
Proximal
Tibia
Distal
Tibia
Distal
Femur
Proximal
Femur
8401R
E*
8410R10
L 3
E
8411R 9
LIO
E*
Talus
MtIII
E
8411R 6 E
8411R 9 P*
E
84121,81-2 E* 8412L 4 E/P*
R 3
P
8412L 7 P*
8412L 3 P*
8412R 6 P*
8412L 10 E*
R 11 E*
P*
P
8419L 2 E*
R5-6 E*
8512R2-3 P
8419L2-3 P*
R 3
P*
8512R2-4 E*
8521R2-4 E*
L2-4 E*
8309R6-8 E*
R 2
L2-3
L2-3
L 6
E*
E*
E*
E*
P*
P*
E
L1-2 P
8507L 4 E
L 5 E*
8507R 6
8602L2-3 E*
8602L 2 P*
L8-9 E*
L2-4 P/E*
8602L 4 P*
8602L 2
8603R2-3 E*
8603L 5 E*
R6-7 E*
L2-4 P/E*
L 6 P*
R3-4 E/P*
L6-7 E*
E*
R 5
L2-3 E*
8603L 4 E*
L 7 E*
R 4 E*
8507R 2
R 7
P/E*
P*
R 3
R 4
L3-4 P/E
8507LB 2 P*
8510L 2
R 2
15
Distal humerus.
25
E*
E*
8510
L 5
8603L
L
L
,
R
R
E*
E*
E*
E*
E*
8603L
L
L
L
L
2
4
4
6
P*
E*
E*
P*
7
P*
8510R 3 E*
4 E/P*
11
3
5
5
7
4
P*
P*
3
6
15
There were 9 epiphyseal lesions in the distal humeral epiphysis;
3
of these were in medial slabs (trochlea) and 6 in lateral slabs (capitulum). The
capitulum lesions were all in its caudal half.
There was one metaphyseal lesion, which had broken through the caudo-lateral
aspect of the metaphysis into the surrounding fascia.
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THE VETERINARY QUARTERLY, VOL. 10, No, 2, APRIL 1988
Proximal
Humerus
84111. 4
Distal
Humerus
Proximal
Radius
Ulna
Distal
Radius
8410R 3
E*
8411R1-2
R 10
L1-3
L 13
R 9
P*
P*
P*
P
P*
8412L 6
P*
8419R5-7 E*
L5-8 E*
8419L 8
E
E
E
R4-6 E
8412L 3
E/P*
8419L2 -3 P*
8412L 7
R 7
8512L 5
8507L 3
8507R 3
E/P*
8507R 3
E/P*
8602L
2
8603R 3
R
R
L
L
9
2
6
6
8411L 8
E
8419R 6
P*
P*
P
R 4
E*
8309R 1
8309L 2
R8-9
R 8
L 8
L 8
E*
P*
E*
P*
E*
8507L 6 P*
8507R
L
R
L
P*
E*
8603L2-6 P/E*
R2-5 P/E*
McIII
3
3
8
8
E
8507R 4
L 4
P*
P
E*
E*
E*
8602R7-8 P*
E*
E*
E*
E*
E*
8603L
R
P*
P*
8603L
L
R
R
R
2
8
2
2
8
R 7
R 8
P*
E*
P*
E*
E*
P*
P*
7903R 2
L 7
E*
P*
8004R 2
P*
8037R 6
P*
R 7
P*
8127R 2
P*
8
8119L 2 P*
L 7 P*
R7-8 P*
10
1
4
8123R 5
P*
8127L 7
P*
34
8
.
103
CA
Fore limb
CR
1
6
Prox. radius
Distal humerus
Proximal humerus
CR
Axial
Lat.
Med.
Lat./Med.
Distal radius
Axial
Distal Mc3
Hind limb
Lat.
Med.
Distal femur
Prox. femur
R
Axial
Med.
CR
DA
A
Lat.
Distal tibia
Prox. tibia
CA
CR
Lat./Med.
Med. ridge
Lat. ridge
Axial
Distal Mt3
Talus
Figure I. Schematic drawings of the sagittal slabs in which most lesions were detected in the bone
ends. The numbers refer to the numbers of lesions found at each site indicated.
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No. 2, APRIL 1988
Ulna. Four lesions were found in the metaphysis of the olecranon, but in all cases
there was either radiographic and/or histological evidence of involvement of both
the metaphysis and the apophysis.
Proximal radius.
One lesion was found in the epiphysis close to the synovial fossa.
Distal radius.
There were 13 lesions in the epiphysis of either the medial process of
the radius (5) or in the lateral styloid process (8). The medial lesions were always at
the junction of cartilage and bone and were always focal; several, but not all, of the
lateral styloid process lesions were demonstrated to be in its most cranial part,
adjacent to the fibrous tissue separating the process from radial epiphysis. In other
cases, the lateral styloid process contained more than one lesion and/or copious
exudate, and extension of the infiltrate into the radial epiphysis and into the distal
radial metaphysis was observed.
The 21 P type lesions were in moste cases found in the inclined parts of the distal
radial growth plate. The localisations were cranial inclination (1), caudal
inclination (1) or both the cranial and caudal inclinations (2) of the growth plate in
the medial aspect of the radius; there were a further 3 lesions at the junction of the
perichondrium and growth plate on the caudal aspect of the bone. On the lateral
aspect of the radius, the sites were the most caudal (5) or more cranial parts of the
growth plate (7) dorsal to the lateral styloid process. In several of the caudolaterally sited lesions, association with infiltrate or lysis in the radial epiphysis or
lateral styloid process was observed. Between the two processes of the radius i.e.
axially, there were 2 lesions on the cranial aspect of the growth plate.
Third metacarpal bone. One epiphyseal lesion was observed just caudal to the
most distal aspect of the convexity of the epiphysis, on the lateral side.
There were 7 metaphyseal lesions in the cranial (4) and caudal (3) inclinations of
slabs lateral (5) or medial (1) to the median sagittal ridge, and 1 of these lesions was
in the central slab containing the median ridge.
Proximal femur. There were 15 lesions detected in 8 bones from 5 foals. There
were 7 lesions in the epiphysis, and 2 of these were adjacent to the insertion of the
round ligament. The other 5 were at the most medio-ventral aspect of the epiphysis,
and all but one of these 5 had involvement on both sides of the growth plate. The
lesions appeared to have originated in the metaphysis.
The other 7 lesions were found at various sites along the metaphyseal growth plate,
and one lesion was in the major trochanter.
Distal femur. There were 25 lesions detected in 18 bones from 11 foals. The most
common site (14 lesions) was in the medial femoral condyle, caudal and dorsal to
the articular contact surface. Five lesions were found in the lateral femoral condyle
at the same level as in the medial condyle. There were 5 lesions in the lateral femoral
trochlear ridge (in its proximal (4) or middle (1) third), and there was one lesion in
the medial femoral trochlear ridge.
Proximal tibia. There was one lesion in an identical site in the lateral part of the
left and right proximal tibial epiphyses of one foal. On the medial aspect of one of
these bones there was a metaphysitis of the proximal tibial growth plate.
Distal tibia. There were 5 lesions in the cranio-distal aspect of the distal
intermediate ridge, and one lesion in the most caudo-dorsal aspect of the ridge.
There was 1 lesion in the fibular styloid process.
Metaphyseal lesions were detected in the cranial inclination (3) and caudal
inclination (1) of the distal tibial growth plate; one of these lesions was lateral, the
other 3 were in the central part of the bone.
THE VETERINARY QUARTERLY, VOL. 10, No. 2, APRIL 1988
105
Talus. There were 5 lesions found in the tali of 1 animal. In both tali there was a
lesion at the junction of cartilage and bone in the distal part of the medial talar
ridge; both lesions were 15 mm from the insertion of the joint capsule. There was a
lesion in the most distal aspect of both lateral talar ridges, and in the left talar ridge
there was an additional lesion in the mid-region of the convexity of this ridge. In
another foal there was one lesion in the mid region of the convexity of the medial
ridge.
Third metatarsal bone. There were 4 epiphyseal lesions, 1 of which was caudal and
3 of which were cranial to the most distal point in the convexity of the epiphysis. All
but one of these lesions were in the median sagittal ridge.
The 11 metaphyseal lesions were in the 'through' (1 lesion) or on the cranial (5) or
caudal (5) inclinations of the growth plate in slabs lateral (6) or medial (5) to the
median sagittal ridge.
In the cases of the epiphyseal lesions in the medial styloid process and lateral
styloid processes of the radius, the medial and lateral condyles and lateral trochlear
ridge of the distal femur, proximal humerus, proximal femur, and intermediate
ridge of the tibia, the site of the lesions in these parts of the bones was in the direct
vicinity of the thickest cartilage in that part of the bone. In some bones, the plane of
sectioning, or bone growth since the time of onset of necrosis, meant that the lesion
was not exactly at the site of thickest cartilage, but within 4-5 mm of it.
Almost all of the P type lesions (metaphysitis) in the distal radius and metacarpus
and metatarsus were on the inclined parts of the growth plate. In the proximal
humerus and proximal femur, the lesion appeared in some cases to have begun in
the metaphysis at a site where it is covered by articular cartilage i.e. in the
centrocaudal part of the bone end. In many subacute lesions, exudate and cells in
transphyseal vessels and on both sides of the growth plate were present. In many
other cases, communication through the growth plate was a result of direct
extension of the lesion through the physeal cartilage.
DISCUSSION
We chose to examine the site of focal osteomyelitis lesions in foals because defining
these sites may contribute to increased knowledge of the pathogenesis of polyosteomyelitis and provide insight into the sites of articular cartilage which should be
especially well evaluated radiologically and arthroscopically in the diagnosis and
treatment of the disease. Ideally, infection experiments would provide more
accurate data, but these were not possible, and we thus resorted to examination of
naturally occurring disease.
Strictly speaking, the definitive diagnosis of bacterial osteomyelitis can be made
only by observing the characteristic histological and radiological changes in tissue
from which pathogenic micro-organisms have been cultured. In examining focal
lesions which have not extended to the outside through bone or cartilage, it is
impossible to culture the lesions before sawing of the bones, because it
is
impossible to predict the site of possible bone lesions without the benefit of clinical
and radiological examinations in vivo. Many of the focal lesions were too small to
have been demonstrated on clinical radiographs in any case, and for this reason,
and due to expense, we did not radiograph the limbs collected from routine post-
mortem cases. Others have expressed the difficulty in diagnosing chronic bone
infection on the basis of histological changes (10). We excluded foals with lesions
which had features of other disease processes (e.g. retained cartilage). Although we
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2, APRIL 1988
proved infection in the joint or bone of only half the foals in this study, we believe
that the combination of clinical and pathological data, the multifocal nature of the
disease in the foals included in the study, and the radiological and histological
features of the lesions observed were sufficient to justify at least a strongly
tentative, if not conclusive, diagnosis of infection as the cause of arthritis and
osteomyelitis in these foals. Of the 140 lesions observed, 119 showed obvious bone
loss on microradiographs or histological preparations. There are no other disease
processes in very young foals which cause multifocal bone and/or cartilage loss.
This meant that the difficulty in making the diagnosis on the basis of chronic
infiltrative changes in affected bone was alleviated. In cases without lysis or
necrosis, the obvious infiltrate of exudate and cells pointed to the presence of
(sub)acute inflammatory change.
The lesions were found at the junction of bone and the metaphyseal growth plate
cartilage, or at the junction of bone and epiphyseal growth cartilage (7,8); (the
latter has also been referred to (9) as the spherical physis or secondary physis to
more precisely indicate that we mean the growth plate by which the epiphysis
expands in all directions i.e. the growth plate surrounding the secondary ossification centre). Siffert (8) has indicated that regardless of their anatomical location,
growth cartilages apparently function in a similar biological manner, and this
supports the use by Nixon (6) of the therm 'metaphyseal equivalent site' to indicate
the significance of the vascular arrangement in the pathogenesis of haematogenous
osteomyelitis in flat bones in man. This vascular arrangement, in which sharp loops
in marrow capillaries open into wide sinusoids and produce sluggish circulation,
has been a constant feature of explanations for the localisation of lesions at the
cartilage/bone junction.
In the distal humerus, the site of the lesions within the capitulum or trochlea was
not constant. In the case of the talus, there were lesions at the site of thickest
cartilage, but also at sites with thinner cartilage. In the case of the medial styloid
process of the radius, femoral condyles, distal tibia, and proximal humerus, it
could be seen that the site of focal lesions was exactly adjacent to the thickest
cartilage on the slabs examined in this study, and these sites have previously been
shown to be the sites of thickest cartilage in the respective parts of the bone end (3).
In the lateral styloid process of the radius and proximal femur, the focal lesions
were close to the thickest cartilage, but not at an absolutely constant site. This may
be due to the small size and rapid rate of enchondral ossification in the lateral
styloid process and to the possible role of the insertion of the round ligament in the
proximal femur. The incidence of epiphyseal lesions found in the proximal radius
and proximal tibia was extremely low (only 4 lesions). The distribution of the
lesions in the various bone ends agrees with a previous study (1), except for the
higher incidence of epiphyseal lesions in the distal humerus, and of lesions in the
proximal femur. The difference in the latter case may be due to the greater difficulty
in examining the hip area in clincial cases. We confirm the known (1) predisposition
sites within some epiphyses such as the site in the lateral and medial femoral
condyles and distal intermediate ridge of the tibia, and present new apparently
predisposed sites (medial styloid process radius, proximal humerus). We presume
the relationship of lesion site and thick cartilage to be associated with local
vascular morphology.
It appeared that more lesions occurred on inclined parts of the growth plate than
on those parts of the physis at 90 degrees to the long axis of the bone. It also
appeared that the lesions were on the most inclined part of the physis, but this
THE VETERINARY QUARTERLY, VOL. 10, No. 2, APRIL 1988
107
could not be substantiated since detailed morphological studies of the developing
equine growth plate are lacking. Because of the greater site variation in the
metaphysis lesions than in the epiphysis lesions, and because of insufficient
numbers, we do not at this time have an explanation for the apparent predisposi-
tion site within a given metaphysis.
This study of focal lesions provided clear evidence of the role of transphyseal
vessels in permitting infection to cross the growth plate, although invasion directly
through cartilage may also occur.
ACKNOWLEDGEMENTS
The authors are extremely grateful to Mr. A. Klarenbeek for his skillful preparation of bone
slabs, radiographs and histological slides. They also thank Mr. F. Blok for illustrative
material and Ms. J. de Graaf-de Hart for developing the radiographs.
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7. Siffert RS. The effect of trauma to the epiphysis and growth
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