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Bacterial chondronecrosis with osteomyelitis
('femoral head necrosis') of broiler chickens:
A review
Perpetua T. McNamee
a
, Joan A. Smyth
a
& Joan A. Smyth
b
a
Veterinary Sciences Division , Department of Agriculture and Rural
Development for Northern Ireland , 43 Beltany Road, Omagh, Co Tyrone,
BT78 5NF, UK
b
Veterinary Sciences Division , Department of Agriculture and Rural
Development for Northern Ireland , 2 Stoney Road, Stormont, Belfast, BT4
3SD, UK
Published online: 17 Jun 2010.
To cite this article: Perpetua T. McNamee , Joan A. Smyth & Joan A. Smyth (2000) Bacterial chondronecrosis
with osteomyelitis ('femoral head necrosis') of broiler chickens: A review, Avian Pathology, 29:4, 253-270,
DOI: 10.1080/03079450050118386
To link to this article: http://dx.doi.org/10.1080/03079450050118386
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ISSN 0307-9457 (print)/ISSN 1465-3338 (online)/00/040253-18 2000 Houghton Trust Ltd
Avian Pathology (2000) 29, 253270
*
To whom correspondence should be addressed. Tel: +44 2882 243337; Fax: +44 28 2442288; E-mail: Perpetua.McNamee@dardni.go v.uk
Received 31 March 2000. Accepted 31 March 2000.
REVIEW ARTICLE
Bacterial chondronecrosis with osteomyelitis
(
femoral head necrosis
)
of broiler chickens:
a review
Perpetua T. McNamee
1
*
& Joan A. Smyth
2
Veterinary Sciences Division, Department of Agriculture and Rural Development for Northern Ireland,
1
43 Beltany Road, Omagh, Co Tyrone BT78 5NF, UK and
2
Stoney Road, Stormont, Belfast BT4 3SD, UK
Bacterial chondronecrosis with osteomyelitis
(
BCO
)
in chickens was first reported in 1972 and is now
recognized as an important cause of lameness in broiler chickens. Recent systematic studies of causes
of lameness in birds reared in Northern Ireland have shown that it was the most common cause of
lameness, being present in 17.3% of lame birds. Furthermore, it was also detected in birds presented
as found dead. Overall losses in male birds due to BCO were estimated to be 0.75% of all birds
placed, which, in addition to welfare concerns, represents considerable economic loss. The disease has
been seen in birds ranging from 14 to 70 days of age, but most cases occurred around 35 days old. It
is most commonly caused by Staphylococcus aureus, but Escherichia coli, coagulase-negative
staphylococci and Enterococcus spp. are sometimes involved, as are, rarely, other bacteria. The lesions
are most commonly found associated with the growth plates of long bones, particularly the proximal
growth plate of the femur and tibiotarsus, but other bones may also be affected. Since lesions were
visible to the naked eye in only 40 to 67% of cases, histological examination is recommended where no
lesions are visible macroscopically. As the lesion may be present in only one growth plate, and because
histological examination is often not carried out, BCO is almost certainly underdiagnosed. The exact
pathogenesis of the condition is unknown, but it is thought that adherence of blood-borne bacteria to
exposed cartilage at the tips of metaphyseal blood vessels is fundamental. Under controlled
experimental conditions, infection of birds with the immunosuppressive viruses chicken anaemia virus
and infectious bursal disease virus increased the incidence of the disease, while restricting feed intake
reduced the incidence of disease. S. aureus strains identical to, or closely related to, isolates recovered
from naturally occurring cases of the disease
(
as determined by pulsed-field gel electrophoresis
)
have
been recovered from fluff-debris in hatcheries, and also from the environment of breeding flocks,
indicating that infection in the breeding farm and in the hatchery could be an important source of
infection. It has also been shown that humans can carry poultry strains of S. aureus on their hands.
There is a higher incidence of BCO in birds hatched from floor eggs. Thus, hygiene and management
practice on breeder farms and in the hatchery may influence the occurrence of the disease.
Bacteraemia is a prerequisite for BCO. Indeed, in some flocks suffering losses due to BCO, there are
also losses due to staphylococcal septicaemia. Thus, appropriate treatment of affected flocks should
reduce losses due to septicaemia. It should also reduce the occurrence of bacteraemia and the
development of further cases of BCO. However, birds in which BCO has already developed, are
unlikely to respond to treatment. Control of BCO by vaccination seems unlikely in the short term.
Simple bacterins have not been effective and much basic research is needed to identify the important
virulence factors. Furthermore, more than one type of bacterium is capable of causing the disease.
Bacterial interference has been used successfully in humans and turkeys to prevent staphylococcal
diseases, and warrants investigation for the prevention of BCO in chickens. This may have an
advantage in that the interfering bacterium may also exclude some of the other bacteria that can cause
BCO. The recent development of a disease model in which S. aureus is given by a natural route allows
the potential for further investigation of the role of predisposing factors, and intervention strategies,
including vaccination and bacterial interference, for the prevention of BCO.
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Introduction
Lameness compromises the welfare of chickens and
causes considerable economic loss
(
Riddell, 1992
)
.
Lame birds have difficulty accessing food and
water, and will therefore become dehydrated and
die. Based on data recorded daily and from weekly
necropsy examination of birds from 51 broiler
flocks in Western Canada, Riddell & Springer
(
1985
)
found the incidence of birds culled due to
lameness to range from 0.46 to 4.08%. In this study,
the average incidence of chickens with skeletal
deformities was 1.72%, which included 1.1%
chickens culled in the field and 0.62% chickens
condemned at processing. A national survey in the
US estimated that leg problems cost the broiler
industry between 80 and 120 million dollars
annually
(
Morris, 1993
)
. Although there have been
several comprehensive reviews describing skeletal
abnormalities of poultry
(
Wise, 1975; Riddell,
1981, 1992; Thorp, 1994
)
, few detailed surveys
(
Randall & Mills, 1981; Riddell, 1983; Riddell &
Springer, 1985
)
have been conducted on commer-
cial chicken flocks to define the incidence and
significance of different disorders
(
Riddell, 1992
)
.
Historically, the majority of conditions cited as
important causes of lameness were of non-infec-
tious aetiology. Osteomyelitis was first reported as
a cause of lameness in commercial broiler chickens
in Australia
(
Nairn & Watson, 1972
)
, and Staphylo-
coccus aureus was shown to be the cause. The
condition, more correctly called bacterial chon-
dronecrosis with ostemyelitis
(
BCO
)

(
see the next
section
)
, has subsequently been reported in broilers
from other parts of Australia, the US, Canada and
Europe
(
Griffiths et al., 1984; Riddell & Springer,
1985; Thorp et al., 1993; Randall & Reece, 1996;
Thorp & Waddington, 1997; McNamee et al.,
1998
)
.
Studies of commercial broilers carried out
between 1965 and 1978 showed that most skeletal
abnormalities causing lameness were associated
with long bone growth disturbances, frequently
involving the growth plate
(
Prasad et al., 1972
)
or
were manifest as bone deformities
(
Poulos et al.,
1978
)
. Subsequentl y, a working party in the UK
(
MAFF/ADAS, 1981
)
identified tibial dyschon-
droplasia
(
TD
)

(
Leach & Nesheim, 1965; Siller,
1970
)
, and angular limb deformities
(
Julian, 1984;
Duff & Thorp, 1985
)
as the predominant causes of
lameness. Studies of commercial broilers in Canada
showed that long bone deformities were the main
cause of lameness, while arthritis and osteomyeliti s
accounted for only 10% of losses due to lameness in
the last week before processing
(
Riddell &
Springer, 1985
)
. The MAFF working party listed
leg disorders in order of priority, and osteomyeliti s
was placed low on this list
(
MAFF/ADAS, 1981
)
.
Over a decade later, a report on the welfare of
broiler chickens
(
Farm Animal Welfare Council,
1992
)
indicated that osteomyelitis was being
increasingly recognized as a cause of lameness in
commercial broiler chickens. A study by Thorp et
al.
(
1993
)
in the UK, which targeted birds suspected
to have a lesion in the hip, showed a high incidence
of BCO. It was also a common diagnosis in lame
birds examined by Thorp & Waddington
(
1997
)
.
BCO was later shown to be the most common cause
of lameness in commercial birds through systematic
large-scale study of lame broilers from seven
commercial flocks
(
McNamee et al., 1998,
1999a
)
.
There have been reports of conditions similar to
BCO in other avian species. The descriptions by
Hole & Purchase
(
1931
)
of abscesses involving the
articular cartilage and long bones of pheasants are
highly suggestive of osteomyelitis, although the
lesions were not examined histologicall y. S. aureus
was recovered from the abscesses. Staphylococcal
osteomyelitis was reported by Jungherr
(
1933
)
in
geese. Naturally occurring bacterial osteomyeliti s
with synovitis was recorded in turkeys in Australia
(
Nairn & Watson, 1972
)
and the US
(
Nairn, 1973
)
;
S. aureus was the most common isolate. Subse-
quently, Wyers et al.
(
1991
)
described osteomyeliti s
associated with S. aureus in male breeding turkeys
in France. Turkey osteomyelitis complex
(
TOC
)
is
an important cause of lameness and of carcase
condemnations in turkeys in the US
(
Bayyari et al.,
1994
)
. The pathogenesis of the condition in turkeys
appears to be very similar to that in chickens,
although TOC is associated with green livers in
turkeys, but not in chickens
(
Mutalib et al., 1983a
)
.
Osteomyelitis caused by S. aureus is also a
significant disease of children
(
Ish-Horowitz et al.,
1992
)
.
This paper reviews the current state of knowl-
edge about the disease in chickens, and describes
salient features of the most commonly involved
bacterium, S. aureus.
Terminology
Over the past few decades, this condition has been
reported under a variety of names; osteomyelitis,
femoral head necrosis, long bone necrosis, proximal
femoral degeneration, bacterial chondritis with
osteomyelitis, and BCO. The latter terms are
considered to be the most appropriate by the present
authors because they describe the pathology most
accurately and also indicate the bacterial aetiology.
The terms femoral head necrosis and proximal
femoral degeneration, while both descriptive, do
not take account of the fact that the lesions may
occur in any bone, and are common in the
tibiotarsus. Furthermore, they may include degen-
erative changes unrelated to bacterial infection
(
Julian, 1985; Duff & Randall, 1987
)
. The term
femoral head necrosis has also been used to
describe lesions associated with malabsorption
syndrome in broilers
(
Page et al., 1981
)
and with
254 P. T. McNamee & J. A. Smyth
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Bacterial chondronecrosis in broilers 255
Figure 1. Commercial broiler, 28 days old. Note wing extended
for support. This is typical in a broiler with bacterial
chondronecrosis and osteomyelitis in the proximal end of the
femur.
Figure 2. Proximal end of the femur, midline frontal section,
28-day-old lame commercial broiler. Note the large zone of
yellow tissue extending from the growth plate region (gp) to the
medullary cavity (mc).
Figure 3. Physeal cartilage in the proximal end of the femur,
midline frontal section, 35-day-old lame commercial broiler.
Note clumps of basophilic bacteria (bb) in metaphyseal blood
vessel surrounded by poorly stained physeal chondrocytes and
matrix (ps), contrasting with the dark blue, normally stained
cartilage (ns) to left and right of photograph, (Haematoxylin &
eosin). Bar = 525 mm.
Figure 4. Hypertrophic chondrocytes (hc) lining metaphyseal
blood vessel (mv) in the proximal end of the femur, midline
frontal section, 35-day-old lame commercial broiler. Clumps of
basophilic bacteria (bb) are seen in a blood vessel and in
chondrocyte lacunae (Haematoxylin & eosin). Bar = 59 mm.
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reovirus infection
(
Van der Heide et al., 1981
)
.
However, the lesions seen in malabsorption syn-
drome were in fact osteoporosis, not necrosis
(
Julian, 1985
)
. Duff & Randall
(
1987
)
found
detachment of the proximal femoral cartilaginous
epiphysis at slaughter, which they proposed was
associated with a traumatic aetiology following
injury at catching. They suggested that the terms
fracture separation or traumatic epiphysiolysis of
the cartilaginous epiphysis are more appropriate
than femoral head necrosis or degeneration to
describe such lesions. In some reports, histological
descriptors were applied to lesions based on their
macroscopic appearance, which is inappropriat e
and potentially inaccurate. Attempts were made by
Julian
(
1985
)
to clarify diagnosis of lesions in the
femoral head, by categorizing them on the basis of
their histological appearance. He distinguished
three types of lesion, i.e. osteochondrosis, dyschon-
droplasia and osteomyelitis in 16- to 30-week-old
male turkeys. The term osteomyelitis is inadequate
because it does not describe the lesion in the growth
plate cartilage in young growing birds.
Clinical Signs
In naturally occurring BCO of the leg bones, birds
may show signs of lameness or may simply be
found dead. The onset of lameness may be
associated with a rising mortality rate in the flock
(
Nairn & Watson, 1972; Griffiths et al., 1984
)
.
Nairn & Watson
(
1972
)
reported that the incidence
of lameness due to BCO in broiler chickens may
reach 50%, with up to 5% mortality of the
flock.
Live affected birds usually have a characteristic
limping gait. When the lesion occurs in the
proximal end of the femur, birds typically use one
or both wing tips for support during locomotion
(
Figure 1
)
or hip flexion, and vocalize loudly when
pressure is applied to the affected region
(
Thorp et
al., 1993
)
. In experimental studies using aerosol
infection with S. aureus, lame birds in isolators
generally became moribund within 8 h, and died
overnight if not removed on the first day of clinical
signs
(
McNamee et al., 1999b
)
. Interestingl y, after
intravenous inoculation of S. aureus to 29-day-old
birds, lameness was generally observed after 2 days
but birds could survive for up to a further 6 days
(
Emslie et al., 1983
)
. After intravenous inoculation
of 26 groups of 45-day-old birds with S. aureus,
Mutalib et al.
(
1983a
)
found that clinical signs
followed a similar pattern in all groups, with ruffled
feathers, reluctance to walk, heads down, closed
eyes, birds sitting on their hocks, and weak
response to external stimuli. A sharp decrease in
feed and water intake ensued, and death usually
followed 2 to 5 days after the first appearance of
signs
(
depending on the dose of inoculum
)
. The
differing survival times after the onset of lameness
in birds exposed to S. aureus by aerosol and by the
intravenous route may be a reflection of differing
age or bodyweight at infection, or perhaps the
differing management conditions used in each
experimental procedure.
In the advanced stages of the disease, affected
broilers are reluctant to move
(
Nairn & Watson,
1972
)
and would therefore be unlikely to obtain
food or water. Weight loss has been recorded as a
feature of both the naturally occurring disease
(
Griffiths et al., 1984
)
and experimentally induced
disease
(
Emslie & Nade, 1985
)
. The negative effect
on growth rate has been used as a predictor of lesion
development with the intravenous model
(
Emslie et
al., 1983
)
.
Age
Nairn & Watson
(
1972
)
found cases in broilers aged
4 to 8 weeks. It was also recorded, together with
arthritis/tenosynovitis, in birds aged from 35 to 45
days by Griffiths et al.
(
1984
)
. Riddell & Springer
(
1985
)
found arthritis and osteomyelitis from 34
days onwards in birds processed from 41 to 49
days. BCO was diagnosed in lame birds aged from
34 to 70 days
(
Thorp et al., 1993; Thorp &
Waddington, 1997
)
. While studying five commer-
cial flocks, McNamee et al.
(
1999a
)
found BCO in
birds aged from 14 to 49 days, with the peak
incidence occurring most frequently at 5 weeks of
age. In experimental studies, where S. aureus was
administered by aerosol, the majority of BCO
lesions developed between days 31 and 40 when
birds were exposed to S. aureus at 1 day old and
infected with immunosuppressive viruses on day 21
(
McNamee et al., 1999b
)
. Thus, the peak incidence
of BCO coincides with the maximum stocking
density of the birds, and is at a time when the
growth plate is rapidly proliferating.
Pathology
Location of BCO lesions
The most commonly affected sites in naturally
occurring cases of BCO in poultry are the proximal
end of the femur and tibiotarsus
(
Nairn, 1973;
McNamee et al., 1998
)
. Lesions occur less fre-
quently in the proximal tarsometatarsus, distal
femur, distal tibiotarsus, proximal end of the
humerus or vertebrae
(
Nairn, 1973; McNamee et
al., 1998
)
. In one study of naturally occurring cases
where all growth plates of the long bones of the legs
were examined histologicall y, lesions were present
only in the proximal end of the femur and in the
proximal end of the tibiotarsus
(
McNamee et al.,
1998
)
. In a subsequent field study where the
proximal end of the femur and tibiotarsus was
examined by histology, the most frequently affected
site was the right femur
(
63.1%
)
followed by right
tibiotarsus
(
40.3%
)
, left femur
(
36.8%
)
and left
256 P. T. McNamee & J. A. Smyth
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tibiotarsus
(
19.3%
)
. Of 57 birds with BCO in the
latter study, lesions were present in all four sites in
21% of birds, in two sites in 15.8% of birds, and in
one site of 63.2% of birds
(
McNamee, 1998
)
. Using
the intravenous model of S. aureus infection in
chickens, Emslie et al.
(
1983
)
found that macro-
scopically visible lesions were most commonly
seen in the proximal end of the tibiotarsus and in the
distal end of the femur of broiler chickens. In that
study, histological examination was not carried out
on other growth plates, so it is possible that lesions
were present at other sites. Mutalib et al.
(
1983a
)
,
who also studied broilers injected intravenousl y,
found that the proximal end of the femur and of the
tibiotarsus were most commonly affected. Lesions
occurred less frequently in the proximal tarsometa-
tarsus, distal femur, distal tibiotarsus and vertebrae
(
Mutalib et al., 1983a
)
. BCO was diagnosed in the
proximal end of the femur, following intravenous
injection of S. aureus to 35-day-broilers by Griffiths
et al.
(
1984
)
, but no other site was examined in this
study. Thorp & Waddington
(
1997
)
reported a
higher incidence of BCO in the proximal end of the
tibiotarsus than in the femur of broilers with
hypophosphataemic rickets.
The real incidence of BCO is likely to be
underestimated during investigation of lameness in
broilers unless the growth plate of the proximal end
of the femur and tibiotarsus of both legs are
examined for lesions. Naturally occurring lesions of
vertebral osteomyelitis, and experimental reproduc-
tion of the condition by intravenous injection of S.
aureus, was reported by Carnaghan
(
1966
)
. How-
ever, the incidence in naturally affected flocks did
not exceed 1%. A lesion of vertebral osteomyelitis
was observed in one out of nine birds with BCO
(
McNamee et al., 1998
)
. One vertebral lesion was
also recorded by Griffiths et al.
(
1984
)
3 days after
intravenous injection of eight birds with S. aureus at
35 days.
In turkeys, Nairn
(
1973
)
found that macroscopic
lesions were evenly distributed in the proximal end
of the femur, the proximal and distal end of the
tibiotarsus, and the proximal tarsometatarsus fol-
lowing intravenous injection with S. aureus.
Lesions consistently occurred in at least two out of
the three sites when the proximal end of the femur,
tibiotarsus and tarsometatarsus was examined. Ver-
tebral osteomyelitis also occurs in naturally infected
and in intravenously injected turkeys, and was
generally found in less than 10% of birds with
lesions in long bones
(
Nairn, 1973
)
.
Macroscopic appearance
At necropsy, birds with BCO were dehydrated and
were generally smaller than non-lame cohorts
(
Emslie & Nade, 1983; McNamee et al., 1999b
)
.
Macroscopically, BCO may appear as focal yellow
areas of caseous exudate or lytic areas, which cause
affected bones to be fragile
(
Skeeles, 1997
)
.
Lesions observed during experimental investiga-
tions varied from a small pale area adjacent to the
growth plate to a large zone of yellow tissue
extending from the growth plate region to the
medullary cavity
(
Figure 2
)

(
McNamee et al.,
1999b
)
. However, it is important to note that many
lesions are only visible using microscopy. Through
several investigations where detailed skeletal exam-
inations were performed, only 40 to 67% of lesions
were visible macroscopically
(
McNamee, 1998
)
.
Lesions observed in naturally occurring cases were
usually larger than lesions observed during experi-
mental investigations
(
unpublished observation
)
.
This may reflect the fact that the experimental birds
were very closely monitored and were therefore
probably culled sooner after onset of lameness than
birds grown under commercial conditions.
In one outbreak of BCO in broilers caused by S.
aureus, fractures of the neck and head of the femur
were observed. In some birds, only one femur had a
thin brittle cortex of the neck region of the proximal
femur and necrotic material in the medullary cavity,
but there was bilateral involvement in others
(
Griffiths et al., 1984
)
. Riddell et al.
(
1983
)
cautioned that separation of the proximal femoral
epiphysis is a common post mortem artefact in
rapidly growing broiler chickens and should not be
called femoral head necrosis unless histological
examination confirms the presence of lesions.
Histological appearance
In BCO lesions developing after exposure to S.
aureus by aerosol, there are usually clumps of
basophilic bacteria in epiphyseal or physeal blood
vessels, and these are surrounded by poorly stained
cartilaginous matrix
(
Figure 3
)
containing necrotic
chondrocytes. Emslie & Nade
(
1983
)
suggested that
the pale staining of the cartilaginous matrix is the
direct result of the degradative effect of bacterial
toxin, produced by S. aureus, on acid mucopoly-
saccharides in the ground substance of the cartilage.
Affected blood vessels may be either completely
occluded by bacteria or contain bacterial clumps
surrounded by inflammatory cells and fibrin
thrombi. Such vessels are usually in the hyper-
trophic zone of the physis and, in this region,
bacteria are also frequently observed in chon-
drocyte lacunae
(
Figure 4
)
. Together with the
cartilaginous lesions, osteomyelitis often occurs in
the metaphysis of the femur and/or tibiotarsus, and
occasionally in the secondary ossification centre in
the proximal end of the tibiotarsus
(
McNamee et
al., 1999b
)
. Early lesions found in cases of field
infection were indistinguishable from those seen in
birds infected by aerosol. More advanced lesions
appeared as large clumps of basophilic bacteria
surrounded by degenerate inflammatory cells and,
in some cases, fibrous reaction. Following intra-
venous infection, Mutalib et al.
(
1983a
)
found acute
and chronic lesions similar to those already descri-
Bacterial chondronecrosis in broilers 257
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bed. In naturally occurring cases of the disease,
while lesions in the proximal end of the femur and
tibiotarsus were invariably detectable on examina-
tion of the first
(
midline frontal
)
section
(
McNamee
et al., 1998
)
, bacterial clumps were sometimes only
found after examination of multiple sections
(
Thorp
et al., 1993; McNamee et al., 1998
)
.
Following a sequential study, Emslie & Nade
(
1983
)
described the sequence of lesion develop-
ment in broilers following intravenous infection as
follows. Bacterial proliferation occluded the vas-
cular tunnels within 24 h. Within 48 h, triangular-
shaped pale lesions bordering on the growth plate
with the apex of the lesion pointing vertically
towards the diaphysis of the bone were observed.
By 48 h, the inflammatory exudate contained many
degenerating cells and numerous secondary foci of
bacteria, and was lined by a dense layer of fibrin.
By 192 h after infection, the dead cartilaginous
matrix harbouring bacteria had frequently formed a
sequestrum that was separated from the surrounding
metaphyseal bone by an oedematous clear zone.
It has been reported that dyschondroplasti c
lesions may act as foci for bacterial necrosis and
subsequent osteomyelitis in turkeys
(
Wyers et al.,
1991
)
, but no evidence of bacterial necrosis was
detected in association with lesions of TD in broiler
chickens by McNamee et al.
(
1998
)
.
Associated lesions in birds or flocks with BCO
There may be concurrent losses due to staphy-
loccoccal septicaemia in flocks affected by BCO
(
Reece, 1992; McNamee et al., 1998
)
. Other
findings in birds with BCO or their cohorts include
arthritis or tenosynovitis associated with the hock
joint
(
Griffiths et al., 1984; Thorp et al., 1993
)
, and
suppurative arthritis of the hip and/or hock joint
(
McNamee et al., 1998
)
. Septic arthritis also
developed occasionally in chickens inoculated
intravenously
(
Emslie & Nade, 1985
)
.
Prevalence of BCO
Pattison
(
1992
)
suggested that the condition des-
ignated femoral head necrosis was the most
common cause of lameness in UK broilers, but also
stated that this terminology encompassed a variety
of gross lesions in the proximal end of the femur
(
infectious and non-infectious
)
. While cases of
BCO have been cited as an important cause of
lameness by other workers
(
Thorp et al., 1993;
Thorp & Waddington, 1997
)
, until the work of
McNamee
(
1998
)
, no study reported the numbers of
birds actually culled or dying due to BCO from
broiler flocks. To obtain an accurate estimate for the
incidence of BCO in commercial broiler flocks, it
was first necessary to determine the total incidence
of birds culled because of lameness
(
lame culls
)
,
and mortalities, and then to determine the incidence
of different disorders contributing to each category.
The number of birds culled because of lameness
and the number of birds found dead was recorded
daily in 28 male and 19 female flocks, selected at
random from two broiler production companies
(
McNamee, 1988
)
. Overall, the mean incidence of
male birds culled due to lameness was 0.52% of 28
flocks, and that of females was 0.38% of 19
flocks.
A detailed longitudinal study of five randomly
selected broiler flocks was then carried out
(
McNamee et al., 1999a
)
. All cull birds and
mortalities occurring on one day each week were
subjected to a detailed necropsy examination, and
the proximal end of each femur and tibiotarsus was
examined by histology
(
McNamee et al., 1999a
)
. A
total of 191 birds culled because of lameness, 138
birds that were found dead, and 89 birds that were
culled for reasons other than lameness
(
other culls
)
were examined. On average, 0.52% of all birds
were culled due to lameness from these flocks. Of
the 191 birds culled because of lameness, BCO was
found in 17.3% of cases, limb deformities in 13.6%,
severe TD in 8.4% and spondylolisthesis in 7.8% of
cases. BCO was present in many of the birds
categorized as other culls, and in birds found dead
in the broiler house. The latter finding suggests that
many birds with BCO are not detected by the
stockman, but subsequently die and are recorded as
mortalities rather than lame culls. Overall, BCO
was diagnosed in 13.7% of the total deaths and culls
(
416 birds
)
examined by histology
(
Table 1
)
.
Therefore, recent work indicates that the ratio of
lameness due to BCO, to lameness of non-
infectious origin, appears to be changing. It is not
known whether this is due to a real increase in the
incidence of BCO, a relative increase compared
with other causes of lameness such as TD and
258 P. T. McNamee & J. A. Smyth
Table 1. Incidence of BCO (diagnosed by histological examination) in birds culled due to lameness, dead birds, other culls, and in
the total number of birds examined from one female and four male commercial broiler flocks (reproduced with permission from
McNamee, 1998)
Total
birds
Total
males
Total
females
Lame
birds
Lame
males
Lame
females
Dead
birds
Other
culls
BCO (%) 13.7 14.4 10.6 17.3 17.2 17.6 12.3 8.0
Number examined 416 341 75 191 157 34 138 87
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An Estimate of Financial Losses due to BCO
In the UK, it was estimated that the condition
designated femoral head necrosis caused a loss
in sales value of 3.78 million to the broiler
industry
(
Pattison, 1992
)
. In that study the term
femoral head necrosis was used to encompass a
variety of gross lesions in the proximal end of the
femur. The work of Thorp et al.
(
1993
)
showed
that of 67 birds exhibiting lameness characteristic
of a lesion in the proximal end of the femur, 61%
had evidence of bacterial infection in this site.
Therefore, by extrapolation, bacterial infection of
the hip may have been responsible for a loss of
approximately 2.3 million in the UK. The mean
incidence of total losses in male flocks was 5.2%
(
McNamee, 1998
)
. It was estimated that BCO
occurred in 17.2% of lame male birds, and in
14.4% of all losses in male birds placed in four
houses
(
Table 1
)
. From these figures, it has been
estimated that for male birds produced in Northern
Ireland, annual losses due to BCO are approx-
imately 185 625. On the basis of the findings
from one female flock
(
McNamee, 1998
)
, losses
due to BCO represent approximately 118 000
annually. By extrapolation, this equates approx-
imately to losses of 3 million due to BCO in
male and female broilers in the UK. These figures
do not include the cost of any treatment that might
have been used, the value of the bird or the cost
of rearing the bird to this age. This cost may be
substantial since the majority of losses due to
BCO occur close to processing.
Bacterial Causes of BCO
S. aureus is the most common bacterium recov-
ered from leg and joint infections of poultry
(
Skeeles, 1997
)
, and it has been frequently recov-
ered from bone infections of commercial broilers
(
Nairn & Watson, 1972; Griffiths et al., 1984;
Randall & Reece, 1996; Riddell, 1997; McNamee,
1998; McNamee et al., 1998
)
. Other bacteria
recovered from infected bone of broilers include
coagulase-positive staphylococci other than S. aur-
eus, e.g. Staphylococcus hyicus, coagulase-neg-
ative staphylococci, e.g. Staphylococcus xylosus
and Staphylococcus simulans, Escherichia coli,
Mycobacterium avium, Salmonella spp. and Enter-
ococcus spp.
(
Reece, 1992; Thorp et al., 1993;
McNamee, 1998; McNamee et al., 1998
)
. The
relative occurrence of these pathogens in cases of
BCO in broiler flocks has been examined in recent
studies in Great Britain and in Northern Ireland
(
Thorp et al., 1993; McNamee, 1998; McNamee
et al., 1998
)
. Thorp et al.
(
1993
)
recovered
bacteria from the proximal femur of birds in
which a lesion suggestive of BCO was evident. Of
the lesions swabbed, coagulase-positive staphylo-
cocci
(
22.2%
)
, coagulase-negative staphylococci
(
11.1%
)
and E. coli or mixed cultures
(
13.3%
)
were recovered. The bacteria were not identified
to species level in that study. Riddell
(
1997
)
reported Staphylococcus spp. as the most common
bacteria isolated from arthritis/tendoniti s/osteomy-
elitis in broilers from Western Canada. He also
noted an increase in the incidence of musculoske-
letal infection associated with E. coli infection.
Bacteriological examination was carried out on
38 bones with BCO, identified during a longitudinal
study of five broiler flocks
(
McNamee, 1998
)
. S.
aureus was recovered from 63.1%, non-haemolyti c
E. coli from 13.1%, Staphylococcus xylosus from
10.5%, S. hyicus from 10.5% and S. simulans from
one lesion
(
2.6%
)
. In another study, S. aureus was
recovered from 62.5% of eight lesions of BCO
(
McNamee et al., 1998
)
. Thus, all the available
information suggests that at this time, S. aureus is
the predominant cause of BCO in commercial
broiler chickens. However, it seems probable that if
measures are introduced which are effective in
controlling/preventing S. aureus infections, other
bacteria will become relatively more common.
However, it remains to be seen whether the actual
incidence of bone infection by the other bacteria
would increase. Ultimately, therefore, attempts to
eliminate BCO will also have to consider the
involvement of bacteria other than S. aureus in the
aetiology of this condition.
Characteristics of S. aureus That May
Influence the Development of BCO
The reason S. aureus causes more cases of BCO
compared with other bacteria is unknown but it may
be a reflection of specific intrinsic characteristics of
the organism. S. aureus is a common, economically
significant pathogen in several species, e.g. it is a
significant cause of mastitis in cattle and sheep
(
Lee, 1996
)
, and of osteomyelitis in children
(
Ish-
Horowitz et al. 1992
)
. S. aureus is a major cause of
hospital-acquired and community-acquired infec-
tion
(
Foster, 1991; Lee & Pier, 1997
)
. The majority
of strains of S. aureus recovered from diseased
humans or animals possess capsules
(
Sompolinsky
et al., 1985; Karakawa et al., 1988
)
. The capsule
impairs phagocytosis and is generally associated
with virulence
(
Jonsson & Wadstrom, 1993
)
. It has
been suggested that the capsule may enhance
adherence to chicken cartilage
(
Speers & Nade,
1985
)
. However, Cunningham et al.
(
1996
)
stated
that the role of capsules in staphylococcal bone and
joint infection, if any, remains unknown.
Gram-positive bacteria such as S. aureus express
surface proteins on their cell wall, which contribute
to virulence by influencing, among other things,
bacterial adherence. Examples of surface proteins of
S. aureus associated with virulence include protein
Bacterial chondronecrosis in broilers 259
angular limb deformities that appear to be decreas-
ing due to breeding selection, or due to increased
awareness of the condition.
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A, fibronectin binding protein, collagen binding
protein, fibrinogen binding protein and bone sialo-
protein
(
Holderbaum et al., 1985; Ryden et al., 1989;
Switalski et al., 1993; Foster & McDevitt, 1994
)
.
Protein A increases the severity of S. aureus
infections by inactivating complement, blocking the
Fc portion of immunoglobulin involved in opsoniza-
tion
(
Kloos & Bannermann, 1995
)
and preventing
the accumulation of neutrophils around bacteria
(
Colburn et al., 1980
)
. A study carried out in an
animal model of peritonitis confirmed that a S.
aureus strain producing protein A was more virulent
than a protein A-negative mutant
(
Patel et al., 1987
)
.
No direct relationship was found between the
production of protein A and the ability to adhere to
tissue by strains recovered from turkeys
(
LeFevre &
Jensen, 1987
)
. However, they suggested that protein
A, when combined with other factors, may contrib-
ute to the ability of S. aureus to cause staphylococcal
infections in turkeys.
Fibronectin-binding deficient mutants of S. aur-
eus have reduced ability to adhere to heart valves in
a rat model of endocarditis, and antibodies raised
against a fusion protein containing regions of
fibronectin offered some protection to cows against
mastitis
(
Foster & McDevitt, 1994
)
. Specific bind-
ing by several strains of S. aureus to collagen was
demonstrated by Holderbaum et al.
(
1985
)
. S.
aureus strains isolated from humans with septic
arthritis or osteomyelitis possessed a collagen
binding receptor
(
Switalski et al., 1993
)
. S. aureus
can bind specifically to several other host proteins,
e.g. bone sialoprotein and fibrinogen binding pro-
tein
(
Foster & McDevitt, 1994
)
, and these may be
important in the pathogenesis of BCO
(
see follow-
ing Pathogenesis section
)
.
The role of cell-surface proteins in the pathogen-
esis of BCO merits further investigation as block-
age of S. aureus adhesion to tissue, perhaps by
production of antibodies to staphylococcal adhe-
sins, might prevent initiation of disease by prevent-
ing adhesion to host tissues.
Source of S. aureus Infection and Methods of
Spread of the Organism
Staphylococcus spp. are normal inhabitants of skin
and mucous membranes of poultry, and are ubiqui-
tuous in environments where poultry are hatched,
reared or processed
(
Steeles, 1997
)
. S. aureus can
be recovered from the skin and nares
(
Harry,
1967a,b
)
, and the dorsal and plantar surface of the
feet of clinically healthy wild birds and chickens
(
Cooper & Needham, 1976
)
. Thus, wild birds may
become infected as a result of contact with poultry
when visiting commercial poultry sites in search of
food, and could potentially act as a reservoir of S.
aureus infection for domestic poultry. S. aureus has
been recovered from litter
(
Vaid et al., 1979
)
, from
feeders and drinkers
(
Vaid et al., 1979; Thompson
et al., 1980
)
, and from the air in poultry houses
(
Vaid et al., 1979; Sauter et al., 1981
)
. S. aureus has
also been isolated from the oral cavity, eye, cloaca
and faeces of healthy chickens
(
Shimizu, 1979
)
, and
from hatcher debris
(
shell, shell membrane, fluff,
etc.
)
and from work surfaces in the sexing and
vaccinating areas, and from the hands of personnel
in hatcheries
(
Thompson et al., 1980; McCullagh et
al., 1998; Rodgers et al., 1999
)
.
During the development of an aerosol model of
BCO, a significantly lower incidence of S. aureus
recovery from birds simultaneously exposed to S.
aureus and inoculated with chicken anaemia virus
(
CAV
)
and infectious bursal disease virus
(
IBDV
)
at
day 21 was observed than that in birds exposed to S.
aureus at day 10 and inoculated with CAV and IBDV
at day 21. Furthermore, 1-day-old chicks exposed to
S. aureus developed a higher incidence of BCO
(
38.4%
)
than 10-day-old chicks exposed to S. aureus
(
8.3%
)
. These findings suggest that broilers may be
at greater risk of developing BCO if exposed at early
stages of the production cycle. In order to test
whether S. aureus recovered from hatcheries might
be a source of organisms causing BCO, 47 isolates of
S. aureus collected from broilers with musculoskele-
tal disease and 62 isolates from fluff samples
collected from chick hatchers were compared using
pulsed-field gel electrophoresis
(
PFGE
)

(
McCullagh
et al., 1998
)
. The PFGE patterns of the isolates
demonstrated either full or closely related identity
between 85% of isolates from clinical sources and
71% of the hatchery isolates. Many of the isolates
from clinical sources had been recovered from
lesions of BCO. The similarity between isolates
recovered from BCO and isolates from the hatchery
confirms that the hatchery is a potential source of
infected birds who develop disease
(
McCullagh et
al., 1998
)
. Therefore, the prevention of S. aureus
contamination in hatchers to avoid colonization of
hatching chicks should be considered an integral part
of the control of BCO.
The possibility of poultry acquiring S. aureus
infection from human contact was investigated by
Harry
(
1967a,b
)
, who identified similar haemolysis
patterns and bacteriophage types in human and
poultry strains. More recently, Hu et al.
(
1995
)
found the same strains of S. aureus in the nares of
adult humans for up to 2 years, confirming that
humans could act as carriers of S. aureus for a long
period of time. Rodgers et al.
(
1999
)
investigated
whether humans could carry poultry-associated
strains of S. aureus capable of causing BCO in
chickens. In this study, personnel from one broiler
hatchery, and workers on 18 separate broiler parent
farms that supply the hatchery, were tested for hand
and nasal carriage of S. aureus. In both types of
location, nasal carriage of S. aureus was more
common than hand carriage, but there was no
evidence of nasal carriage of poultry-associated S.
aureus strains by humans. Hand carriage was
detected in parent farm personnel but not in
hatchery personnel, and some of the S. aureus
260 P. T. McNamee & J. A. Smyth
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strains had identical or closely related PFGE
patterns to strains causing BCO. This raises the
possibility that handling may contribute to the
dissemination of S. aureus associated with BCO in
broilers
(
Rodgers et al., 1999
)
.
Pathogenesis
Much information on the pathogenesis of BCO has
been obtained through observations of the naturally
occurring disease and by studying experimental
models of BCO. Many similarities exist in the
development and maturation of avian and mamma-
lian growth plates
(
Howlett, 1979
)
, and therefore
the broiler chicken has been used extensively as a
model for acute haematogenous staphylococcal
osteomyelitis of human infants
(
Emslie & Nade,
1983, 1985; Emslie et al., 1983; Speers & Nade,
1985; Alderson et al., 1986; Daum et al., 1990
)
.
This model uses intravenous inoculation of bacteria
that, although unlikely to occur naturally in broilers,
nonetheless yields useful information.
Attempts to determine the most likely natural
route of infection in poultry have resulted in
conflicting hypotheses. Smith
(
1954
)
proposed that
staphylococcal infection was likely to be associated
with husbandry conditions in which wounding,
particularly of the feet, was likely to occur. After
hatching, the open navel is a possible portal of entry
for S. aureus
(
Harry, 1957
)
. Insect bites
(
Hinshaw
& McNeil, 1952
)
, cuts in the skin
(
Hole &
Purchase, 1931
)
, and abrasions, vaccination or
minor surgical procedures are all possible routes of
S. aureus entry into the bloodstream
(
Jensen et al.,
1987; Steeles, 1997
)
. Interestingl y, Riddell
(
1997
)
noted an increase in the incidence of musculoskele-
tal infection, including osteomyelitis, associated
with E. coli infection, which he suggested was
associated with an increase in the incidence of
cellulitis due to abdominal scratching. Similarities
were found by Harry
(
1967a
)
between strains of S.
aureus recovered from skin, upper respiratory tract
and bone lesions, and he suggested that staphylo-
coccal infections may occur following mechanical
damage, or disease which favours tissue invasion,
in previously colonized birds. A low percentage
(
10.0%
)
of 10 chickens developed osteomyelitis
when a high challenge of S. aureus organisms
(
5
10
11
)
was given intratracheally in a single dose,
compared with 100% in 10 birds after a lower
challenge
(
5 10
6
)
was given intravenously
(
Mutalib et al., 1983b
)
. Only the 10 birds exposed
to S. aureus by the intratracheal route were
colonized by S. aureus in the respiratory tract. This
work showed that tracheal inoculation with S.
aureus may result in respiratory tract colonization
but the authors suggested that additional, uni-
dentified factors are necessary to induce invasion
and subsequent BCO. An observation by Riddell,
cited in the publication of Mutalib et al.
(
1983a
)
,
indicated that outbreaks of osteomyelitis were
associated with stressful situations such as severe
feed restriction, poor nutrition, overcrowding in
chickens and adverse weather conditions in turkeys.
However, although they were unable to demonstrate
a relationship between the occurrence of osteomye-
litis and stress under experimental conditions,
Mutalib et al.
(
1983a
)
suggested that stress might
initiate outbreaks in chickens that have a latent
staphylococcal colonization from an early age.
Jensen et al.
(
1987
)
suggested that staphylo-
coccal infections did not result primarily from
injection of the organism due to injury, insect bites
or cuts to the skin, rather that the respiratory tract
was the most likely portal of entry of S. aureus in
poultry on the basis of preferential S. aureus
adherence to cells of the respiratory tract compared
with cells from other tissues. Such adhesion of S.
aureus to the surface of the host cell has been
shown to be important in bovine mastitis and
endocarditis in humans
(
Foster, 1991
)
, in human
osteomyelitis
(
Ryden et al., 1989
)
and in osteomye-
litis in chickens
(
Alderson & Nade, 1987
)
.
In studies carried out during the development of
a model of BCO
(
McNamee et al., 1999b
)
, S.
aureus was recovered from the nasal cavity of birds
6 weeks after exposure to the bacterium by aerosol
at 1 day old. Interestingly, the number of birds with
S. hyicus infection of the nasal cavity after 6 weeks
was much lower under the same experimental
conditions. Perhaps S. aureus has an enhanced
ability to adhere to the mucosa of the nasal cavity,
which may increase the opportunity for bacterial
invasion and subsequent bacteraemia. Such an
ability, if present, could contribute to the dominance
of S. aureus as a cause of BCO. Therefore,
investigation of the role of the earlier described
adhesion factors in poultry is warranted.
Injection of S. aureus intravenously
Since bacteraemia appears to be necessary for the
development of BCO, much work has been carried
out studying disease development, by injecting S.
aureus intravenously. In 1973, Nairn found that
intravenous injection of turkeys with S. aureus or
with E. coli produced osteomyelitis indistinguish-
able from that seen in the spontaneous disease. He
concluded that osteomyelitis commenced in the
terminal vessels of the growth plate, and that the
turkey or chicken would make a satisfactory model
for the study of the disease in humans. Subse-
quently, S. aureus was injected intravenously in
broilers
(
Emslie & Nade, 1983; Emslie et al., 1983;
Alderson et al., 1986; Daum et al., 1990
)
as a model
of acute haematogenous staphylococcal osteomyeli-
tis in infants. Studies using this model suggest that
osteomyelitis is caused by the spread of bacteria
from small foci of infection in the growing ends of
metaphyseal blood vessels in the hypertrophi c
region of the cartilaginous growth plate
(
Emslie &
Nade, 1983; Alderson et al., 1986
)
. Howlett
(
1980
)
Bacterial chondronecrosis in broilers 261
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carried out a detailed ultrastructural examination on
the proximal growth plate of the tibia of birds
perfused intravenously with Tyrodes solution. In
the hypertrophic region, it was found that chon-
drocyte lacunae are opened by chondroclasts and
the thin walled metaphyseal blood vessels expand
into them forming small vascular saccules
(
Howl-
ett, 1980
)
. At the advancing capillary tips of
metaphyseal vessels, the attenuated endothelium is
fenestrated and frequently discontinuous, and it was
suggested that these gaps facilitate contact between
bacteria and the physeal cartilage matrix
(
Howlett,
1980; Emslie & Nade, 1985
)
. Howlett
(
1980
)
proposed that blood-borne elements such as bacte-
ria and red cells often extravasate through such gaps
into the extravascular tissues. Sluggish circulation
in the tips of the long narrow metaphyseal vessels
of the growth plate
(
Trueta, 1959
)
may facilitate the
accumulation of bacteria in this region and the
establishment of bacterial infection
(
Thorp et al.,
1993
)
. In addition, broilers fed ad libitum spend a
large proportion of their time in the sitting position,
which may lead to blood flow restriction and poor
circulation to this area
(
Thorp, 1988
)
. In addition to
poor circulation, Thorp et al.
(
1993
)
also cited a
deficiency of macrophages in cartilage and the
rapid formation of occlusive thrombi as reasons for
localization of bacteria in metaphyseal vessels.
Nade & Speers
(
1987
)
and Alderson & Nade
(
1987
)
suggested a specific tropism of S. aureus for
the growth plate cartilage and the articular cartilage
of long bones. Histological studies revealed that
transphyseal blood vessels, connecting the met-
aphyseal and physeal vessels to the epiphyseal
vessels, were present in growing chickens and were a
likely explanation for concurrent acute osteomyeliti s
and adjacent joint infection due to extension of
infection from the metaphyseal blood supply
(
Alder-
son et al., 1986
)
. Using the intravenous model of
BCO, osteomyelitis and septic arthritis due to S.
aureus was produced only in broiler chickens that
were continuously bacteraemic
(
Daum et al., 1990
)
.
It was also found that continuously bacteraemic
chicks developed osteomyelitis.
Ultrastructural studies showed that S. aureus was
anchored to collagen fibres of exposed cartilage
matrix by the extensive network of S. aureus
glycocalyx in the metaphyseal region of long bone
growth plates, but were not adherent to adjacent
vascular linings or red blood cells
(
Speers & Nade,
1985; Alderson et al., 1986
)
.
Inoculation of S. aureus via aerosol
Attempts by Devriese et al.
(
1972a
)
to reproduce
BCO using a suspension of S. aureus by aerosol
resulted in colonization of the upper respiratory
tract from 3 and 14 days, respectively, until 7 and 8
weeks of age without pathological changes in the
skeleton. Several subsequent attempts to reproduce
BCO using S. aureus by aerosol in broilers also
proved unsuccessful
(
Mutalib et al., 1983b
)
, despite
the additional stresses of wetting and chilling.
Jensen et al.
(
1987
)
found that the lung and liver of
19-day-old turkeys became colonized by S. aureus
following aerosol exposure to this pathogen. They
concluded that the presence of liver infection
indicated passage of the bacteria from the respira-
tory tract into the blood or lymphatic system,
although the exact mechanism of spread was not
determined. In a subsequent study, Nicoll & Jensen
(
1987a
)
exposed 14-day-old leghorn chicks to S.
aureus by aerosol, and again found evidence of
colonization of lung and liver tissue following
bacterial culture of portions of each tissue. No
evidence of clinical disease was detected. They
hypothesized that factors exist under field condi-
tions which upset the hostpathogen balance, thus
resulting in clinical disease.
A series of experiments was recently designed in
an attempt to reproduce BCO in broiler chickens
using the aerosol route of infection
(
McNamee,
1998; McNamee et al. 1999b
)
. Birds in isolators
were exposed to a suspension of S. aureus by
aerosol, or exposed to S. aureus and subsequently
inoculated with CAV alone, or with CAV and IBDV.
In all groups, some birds became lame, BCO was
confirmed and S. aureus was recovered
(
McNamee
et al., 1999b
)
. The incidence of BCO was higher in
birds receiving the viruses than in birds exposed to
S. aureus alone. These findings support the hypoth-
esis of Thorp et al.
(
1993
)
, who suggested that
viruses with potentially immunosuppressive effects
might have a role in the development of BCO in
broilers. It is difficult to say exactly why exposure
to S. aureus administered by aerosol
(
in the absence
of viruses
)
produced clinical disease in these
experiments, when others were unsuccessful. Per-
haps the possession of virulence factors by the
strain of S. aureus used, particle size of the
aerosolized inoculum, broiler genotype, or hatching
and rearing environment may have contributed to
the success of the model described
(
McNamee et
al., 1999b
)
.
During these experiments, CAV and IBDV were
given at day 21 and it was found that reducing the age
at which the birds were exposed to S. aureus
increased the incidence of BCO and bacterial
recovery
(
McNamee et al., 1999b
)
. In one of these
experiments, birds fed 100% of the recommended
feed intake for the breed developed a 68.7%
incidence of S. aureus infection and/or BCO, while a
significantly lower incidence
(
10%
)
developed in
birds fed 60% of the recommended intake. However,
feed restriction to such an extent is not a practical
option for the control of BCO in broilers.
McNamee et al.
(
1999b
)
found the highest
incidence of BCO
(
36.8%
)
occurred when 1-day-
old broilers were exposed to S. aureus by aerosol,
and subsequently inoculated with CAV and IBDV
at day 21, while fed ad libitum. Using this model,
birds of a more slow-growing genotype were
262 P. T. McNamee & J. A. Smyth
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investigated
(
McNamee, 1998
)
. Although S. aureus
colonized the nasal cavity of the birds, no BCO
developed. The reason for this is unknown, but it
may be that in the slower growing bird, the
endothelial gaps previously described in the met-
aphyseal blood vessels did not develop signifi-
cantly, thus limiting the possibility of bacterial
invasion and adherence to cartilage in this region.
This might also explain why clinical signs failed to
develop in the studies of Nicoll & Jensen
(
1987a
)
,
who also used leghorns.
Floor eggs
Sparks
(
1994
)
proved a positive relationshi p
between faecal contamination of the egg at ovi-
position and bacterial contamination of the egg-
shell. Eggshells are most susceptible to penetration
by bacteria at oviposition
(
Sparks & Board, 1985
)
.
Therefore, the microbiological status of the envi-
ronment into which eggs are laid influences the
incidence of bacterial contamination of the egg
(
Bruce & Drysdale, 1994
)
. Thus eggs may be
colonized by S. aureus, through contact with faeces
carrying S. aureus. Such eggs may play an impor-
tant role in the dissemination of strains of S. aureus
with the potential ability to cause skeletal infection
to newly hatched broiler chicks. Eggs laid by
broiler parents outside the nest-boxes on the litter-
covered floor are known as floor eggs. Their
incidence is generally highest at the onset of
production and declines to a minimum shortly after
peak production
(
Wilson, 1996
)
.
McNamee
(
1998
)
examined birds hatched from
floor eggs for BCO and by bacteriological culture.
Following culture of bones, S. aureus
(
12.5%
)
and
S. hyicus
(
12.5%
)
were recovered from birds
hatched from floor eggs, and Enterococcus spp.
(
12.5%
)
only from birds hatched from nest eggs.
There was a significantly higher incidence of birds
with bacterial infection of the bone and/or BCO in
birds hatched from floor eggs compared with birds
hatched from nest eggs. The results of this study
suggest that use of floor eggs should be dis-
continued. If they must be used, they should be
incubated separately from clean eggs in an
attempt to reduce the likelihood of contamination of
chicks derived from clean eggs.
Non-bacterial factors that may influence the
development of BCO due to S. aureus
S. aureus is an opportunistic pathogen
(
Jensen et
al., 1987
)
that frequently colonizes healthy chick-
ens, and it appears that under field conditions,
factors exist that upset the hostpathogen balance
in some birds, resulting in the development of
clinical disease
(
Nicoll & Jensen, 1987b
)
.
Several authors have suggested that the occur-
rence of trauma or pre-existing pathology of the
growth plate cartilage may contribute to the onset of
osteomyelitis and BCO. It was noted that osteomye-
litis most frequently occurs in the growth plate of
the distal end of the femur, humerus and radius of
foals where shear forces and focal clefts predom-
inantly occur
(
Firth & Goedegebuure, 1988
)
. Thorp
et al.
(
1993
)
suggested that pre-existing pathology
in the presence of a bacteraemia might predispose
the cartilage to bacterial infection. In order to
examine this hypothesis, the incidence of physeal
osteochondrosis and the incidence of bacterial
infection were examined in lame and sound broilers
(
McNamee et al., 1998
)
. No significant differences
were found between the overall incidence of mild,
moderate or severe physeal osteochondrosi s
between lame and sound birds examined in this
study. It is therefore unlikely that this condition
alone contributed to the lameness observed. How-
ever, significantly more bacterial isolates were
recovered from the bone of the lame birds than from
the bone of sound birds. This difference, together
with the fact that the condition was just as common
in the sound birds, suggests that bacterial infection
was associated with lameness, but not with physeal
osteochondrosis.
The report of the Farm Animal Welfare Council
(
1992
)
cited arthritis and tenosynovitis due to viral
infection
(
Jones et al., 1975
)
as important causes of
lameness. The possible involvement of viruses in
the aetiology of BCO was investigated by
McNamee et al.
(
1998
)
, who found that although
virus isolation procedures yielded adenovirus and
reovirus isolates from bone samples, there was no
association between the occurrence of virus and
skeletal lesions. Thorp et al.
(
1993
)
also recovered
adenovirus and, more surprisingly, infectious lar-
yngotracheitis virus from the proximal end of the
femur. They considered it unlikely that either was
involved in the changes in the joint or bone.
Heterophils collected from commercial broilers
with osteomyelitis due to S. aureus infection had
reduced chemotactic ability
(
Andreasen et al.,
1993
)
. The latter is an important factor in the fight
against bacterial infection. Santivatr et al.
(
1981
)
have shown that IBDV infection affects the ability
of avian heterophils to phagocytose S. aureus,
although the exact mechanism involved was not
determined. Yuasa et al.
(
1980
)
suggested that a
more profound suppression of the immune response
might occur when chicks are infected with both
CAV and IBDV compared with CAV or IBDV
alone. During the development of the aerosol model
of BCO, it was found that dual infection with CAV
and IBDV after S. aureus exposure, compared with
S. aureus only, increased the number of lesions
produced and reduced the age at which BCO
developed
(
McNamee et al., 1999b
)
. Therefore,
CAV and IBDV together play an important role in
the pathogenesis of BCO, although the precise
contribution of each has not been investigated. Any
attempt to reduce the incidence of BCO in broiler
flocks should consider the role of these agents.
Bacterial chondronecrosis in broilers 263
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Hypophosphataemic rickets may influence the
pathogenesis of BCO. Thorp & Waddington
(
1997
)
suggested that an increased likelihood of bacterial
infection of the metaphyseal region of the growth
plate of the tibiotarsus might be related to a relative
phosphorus deficiency. Such a deficiency leads to
elongation of metaphyseal blood vessels within the
elongated degenerating hypertrophic zone. The
increase in blood vessel length may compromise the
blood circulation, allowing bacteria to localize in
this area of poor circulation
(
Thorp & Waddington,
1997
)
.
Of all intensive animal-housing systems, bacteria
appear to be most abundant in poultry housing
(
Sauter et al., 1981
)
. These workers identified S.
aureus as one of the most common bacteria, and
also found that greater numbers of airborne micro-
organisms occurred with higher bird density. Poul-
try house dust contains feed, faecal particles,
bacteria, viruses, feather and skin debris, and litter
particles, which may all cause respiratory insult
(
Whyte, 1993
)
. Ammonia build-up is also a poten-
tial problem in poultry housing
(
Whyte, 1993
)
. No
work has yet been carried out to examine the effect
of various levels of airborne S. aureus or aerial
pollutants such as dust or ammonia on the incidence
of BCO in broiler flocks. It is worth noting that the
younger the bird is when exposed, the greater the
likelihood of it developing BCO
(
see earlier
)
and
the number of air-borne bacteria may be high in
hatcheries. The effect of environment and manage-
ment on the incidence of BCO in broilers has not
been examined to date.
Diagnosis
BCO should be considered in the differential
diagnosis when there is evidence of increasing
mortality within a broiler flock and clinical signs of
lameness in birds of 14 days and older. While some
lesions suggestive of osteomyelitis are visible
macroscopically, many lesions are only detectable
by histological examination
(
Emslie et al., 1983;
McNamee et al., 1999b
)
. To be reasonably sure of
detecting lesions, it is necessary to examine four
growth plates, i.e. both the right and left proximal
femur and tibiotarsus. Histology of the bone is
necessary if no gross lesions are visible, and is also
recommended to confirm the nature of any gross
lesions. If histological examination is not per-
formed in the absence of gross lesions, then the
disease may remain undetected.
Clinical signs caused by vertebral osteomyeliti s
may resemble those caused by spondylolisthesi s
(
Wise, 1975
)
; therefore, a presumptive diagnosis
should be confirmed by bisection of the spine.
It is advisable to culture any suspect lesions, at
minimum using blood agar incubated aerobically at
37C, and also to type the bacterium recovered. The
results will help in the selection of treatment and
control measures if appropriate. Many workers
swab the surface of the lesion and smear this onto
culture medium. However, McNamee et al.
(
1998
)
found that a more successful method for recovering
bacteria was to bisect the target bone
(
in a mid-line
frontal plane
)
, processing one-half for histology,
and to crush the remaining portion in saline for
bacteriological examination
(
McNamee et al.,
1998
)
. Colonies of S. aureus of mammalian origin
generally produce alpha and beta haemolysins,
which cause a zone of clear haemolysis surrounded
by a zone of partial haemolysis when incubated on
ovine or bovine blood agar
(
Quinn et al., 1994
)
.
Poultry strains, however, frequently produce alpha
and delta haemolysins
(
Harry, 1967a
)
. Antibiotic
supplemented medium for the selective isolation of
S. aureus and streptococci may be used as it is
inhibitory to Staphylococcus albus, Micrococcus
spp., and Gram-positive and Gram-negative rods
(
Staph/Strep selective medium SR 70; Oxoid,
Basingstoke, UK
)
.
The majority of strains of S. aureus recovered
from diseased humans or animals possess capsules
that impair phagocytosis and are generally asso-
ciated with virulence
(
Jonsson & Wadstrom, 1993
)
.
Serological typing of the capsular polysaccharides
and, identification of 11 antigenically distinct
capsular polysaccharides for S. aureus has been
described by Karakawa et al.
(
1988
)
. Capsular types
5 and 8 account for 80% of isolates from humans
with bacteraemia. These types also predominate in
milk samples from cows and, in a recent study,
capsular type 5 accounted for 91% of chicken
isolates
(
Daum et al., 1994
)
. PFGE has proved a
useful method to discriminate strain types of S.
aureus recovered from BCO
(
McNamee, 1998
)
.
In human medicine and in veterinary medicine,
radiography is used for diagnosis of osteomyelitis
(
Deysine et al., 1976; Mortensson et al., 1988;
Daum et al., 1990
)
. It has been used to investigat e
lesion development in studies in chickens using the
intravenous model of osteomyelitis. However, it
was found that lesions were not detectable radio-
graphically until 8 days after intravenous injection
of S. aureus
(
Emslie et al., 1983
)
. Therefore, not
only is this technique rather impractical for routine
use in modern broiler production, but it also was not
very effective. In the dead bird, careful macroscopic
examination of bone is likely to identify suspect
lesions at an earlier stage than radiography of the
live bird. Bone scintigraphy, to locate increased
uptake of radionuclide in damaged bone, has been
used successfully to diagnose osteomyelitis in
children and has several advantages over radiog-
raphy. These include the ability to detect early
lesions throughout the body, particularly those in
areas that are difficult to radiograph
(
Mortensson et
al., 1988
)
. However, this technique would be
impractical and too expensive for routine use in
chickens. Daum et al.
(
1990
)
found roentgenog-
raphy was unsuccessful as a method to diagnose
osteomyelitis.
264 P. T. McNamee & J. A. Smyth
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Treatment
Dolman
(
1955
)
stated that among the more chasten-
ing chapters in the annals of microbiological research
is the story of our apparently dismal failure to control
the depradations of the staphylococcus . S. aureus is
inherently a rather resistant organism; many strains
produce penicillinases and infections have always
been difficult to treat. In Belgium, Devriese et al.
(
1972b
)
found that 80% of strains of S. aureus strains
recovered from arthritis/synovitis in broiler breeders
were resistant to penicillin G, 50% were resistant to
tetracycline, and 10% to streptomycin. As in other
species, antibiotic resistance to isolates of S. aureus
from commercial poultry is common
(
Devriese,
1980
)
. Erythromycin-resistant strains of S. aureus
were recovered from outbreaks of dermatitis and
synovitis in chickens
(
Witte & Kuhn, 1978
)
.
Takahashi et al.
(
1986
)
reported that 80% of S. aureus
strains recovered from poultry infections were
resistant to ampicillin, oxytetracycline, erythromy-
cin, kanamycin, streptomycin, chloramphenicol and
sulphadimethoxin. Systemic S. aureus infections in
poultry have been treated successfully with a range of
drugs including penicillin, streptomycin, tetracy-
clines, erythromycin, novobiocin, sulphonamide,
lincomycin and spectinomycin. Reece
(
1992
)
cau-
tioned that antibiotic treatment might limit the spread
of S. aureus in the flock or suppress systemic disease
before osteomyelitis develops, but will not cure
poultry with advanced lesions of BCO.
The general trend towards increasing resistance to
antibiotics is a worrying development in human and
veterinary medicine, and S. aureus is among the
bacteria where problems have been developing. In
human medicine, there has been a dramatic increase
in disease associated with methicillin-resistan t
strains of S. aureus worldwide
(
Kluytmans et al.,
1997
)
. The first detection of methicillin-resistance in
coagulase-negative staphylococci recovered from
chicken in Japan is of concern to the poultry industry
(
Kawano et al., 1996
)
and the situation should be
monitored. The evidence of widespread resistance of
S. aureus to antibiotics indicates that sensitivit y
testing is essential when treatment regimens are
being considered for clinical infections.
Response to treatment of staphylococcal diseases
in other species, e.g. bovine mastitis, is poor
(
Lee,
1996
)
, and the prevalence of antibiotic resistance
among clinical isolates of S. aureus from humans is
high. Human staphylococcal infections and bovine
mastitis due to S. aureus are significant concerns, and
so vaccine strategies to control staphylococcal
infections are being considered and research is well
underway
(
see later and Lee, 1996; Lee & Pier,
1997
)
.
Prevention and Control of BCO
As discussed in the previous section, the use of
antibiotics is unlikely to provide a long-term
solution to the problem of staphylococcal infec-
tions, due to the inherent resistance of the organism
and the concerns over increasing development of
antibiotic resistance. There have been difficulties in
treating and controlling other staphylococcal-asso-
ciated diseases, e.g. osteomyelitis and joint infec-
tions in humans, and mastitis in cattle. By analogy,
the control/prevention of BCO due to S. aureus in
chickens will not be straightforward. There are
three possible approaches to control.
Vaccination
To date, the use of vaccines in the fight against
staphylococcal infection in avians has had poor
success. Jungherr & Plastridge
(
1939
)
had no
success with an autogenous bacterin of S. aureus to
prevent staphylococcal septicaemia and arthritis.
Smith
(
1954
)
, using a live S. aureus vaccine, had
only limited success, and birds inoculated intra-
venously with S. aureus developed lesions in bone
and in other sites.
Currently, there are intensive efforts to develop
S. aureus vaccines for the prevention of bovine
mastitis and human S. aureus infections. Knowl-
edge gained from these studies may be relevant to
the poultry problem. Whole-cell vaccines against S.
aureus infection were unsuccessful in rabbit mod-
els of catheter-induced endocarditis
(
Greenberg et
al., 1987
)
and in humans undergoing peritoneal
dialysis
(
Poole-Warren et al., 1991
)
. Whole-cell
vaccines expressing pseudocapsule were found
to provide a significant level of protection to
lactating ewes and cows against staphylococcal
mastitis
(
Watson, 1992
)
. Encapsulated bacteria are
resistant to phagocytosis by leukocytes, antibodies
specific for the capsule promote phagocytosis of S.
aureus by human leukocytes
(
Karakawa et al.,
1988
)
. It has been suggested that capsular poly-
saccharides conjugated to protein carrier molecules
may lead to an improved immune response
(
Lee,
1996
)
. Systemically administered cellular vaccines
are associated with adverse effects and because of
this, Lee & Pier
(
1997
)
suggested that it was
important to identify surface-associated antigens
which can serve as targets for protective antibodies.
Adhesion of S. aureus to the surface of the host cell
has been shown to be important in bovine mastitis,
and Lee
(
1996
)
reported on the successful reduc-
tion of the incidence of mastitis, through the
production of antibodies by a subcellular vaccine
containing fibronectin-binding protein, in a mouse
model of S. aureus mastitis. To date, a cell-surface
protein that binds fibronectin has been purified, and
the gene has been cloned and sequenced. The role
of this and other binding proteins in bacterial
adherence in vivo could be examined by comparing
the virulence of deletion mutants lacking the
specific binding protein in suitable infection mod-
els
(
Foster, 1991
)
. Many problems are likely to be
encountered during vaccine development since
humans with chronic staphylococcal infection such
Bacterial chondronecrosis in broilers 265
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as osteomyelitis demonstrate a poor immunologi c
response; furthermore, there is no evidence that
patients who recover from S. aureus infections are
immune to re-infection
(
Lee & Pier, 1997
)
. To
develop a successful novel vaccine, a good knowl-
edge of virulence factors would be needed, and this
is lacking for poultry.
Using the aerosol model of BCO, the incidence
of BCO was higher in birds exposed to S. hyicus
and infected with CAV and IBDV
(
23.1%
)
than in
birds exposed to S. hyicus
(
9.1%
)
without viruses
(
McNamee, 1998
)
.
It is also important to remember that vaccination
against S. aureus alone may be of limited use in the
prevention of BCO, since other bacteria can cause
the condition, and may result in a higher incidence
of BCO due to other opportunistic pathogens
particularly when birds are immunosuppressed.
Management
At the present time, the main bacterium found in
cases of BCO is S. aureus, accounting for 62 to
63% of cases in recent surveys
(
McNamee 1998;
McNamee et al. 1998
)
. Using the aerosol model of
the disease, McNamee et al.
(
1999b
)
showed that
the younger the birds were on exposure to S.
aureus, the higher the incidence of BCO. McCul-
lagh et al.
(
1998
)
showed that S. aureus could be
recovered in high numbers in hatcheries, so clearly
exposure of chicks in the hatchery represents a
significant risk. Thompson et al.
(
1980
)
and
McCullagh et al.
(
1998
)
suggested that appropriate
disinfection and improved hatchery hygiene prac-
tices might reduce the levels of initial S. aureus
colonization of chicks. Rodgers et al.
(
1999
)
highlighted the potential importance of hand car-
riage in the dissemination of S. aureus in broiler
parent farms. Personnel should regularly use a
bacteriocidal hand-wash, as part of their general
disease biosecurity measures, to limit carriage and
spread of S. aureus. Continuous bacteriological
monitoring in hatcheries using selective staphylo-
coccal media to give early warning of potential
problems should be carried out
(
J. McCullagh,
personal communication
)
.
Use of the aerosol model has also shown that
exposure to the immunosuppressive viruses CAV
and IBDV increases the incidence of BCO
(
McNamee et al., 1999b
)
. Effective control and
prevention strategies for these viruses is therefore
important. It has also been shown that birds hatched
from floor eggs have a higher incidence of BCO and
bacterial infection, so these should be avoided.
Birds that were growing less quickly had a lower
incidence of BCO, so, theoretically, the incidence
of BCO could be reduced if broilers were not
allowed to grow to their maximum potential. An
examination of the effects of feed restriction at
differing times in the production cycle may be an
area worthy of further investigation.
Bacterial interference
One strategy that has been successfully used to pre-
vent virulent staphylococcal infection both in human
nurseries
(
Kluytmans et al., 1997
)
and in turkey
flocks
(
Jensen et al., 1987
)
is bacterial interference.
Bacterial interference, using S. aureus strain 502A,
was used successfully in human nurseries to curtail
epidemics of S. aureus infection and to interrupt
cycles of recurrent furunculosis in adult humans
(
Aly et al., 1974
)
. Staphylococcus epidermidis has
been used successfully when administered by aero-
sol, both experimentally and in larger-scale control
programmes, to reduce the incidence of S. aureus
infections in turkeys
(
Meyers & Jensen, 1987; Nicoll
& Jensen, 1987b
)
. Preliminary studies of bacterial
interference to control staphylococcal infections in
chickens have also proved successful
(
Nicoll & Jen-
sen, 1987a
)
. The mechanism of interference is
thought to be a function of both competition by the
interfering bacterium for the same tissue receptor
sites and the secretion of a bacteriocin that is bacter-
iocidal for S. aureus
(
Wilkinson & Jensen, 1987
)
.
This approach is worthy of further investigation as a
potential method to control BCO in chickens, and
may have the advantage of interfering with other
bacteria that can cause BCO.
Conclusion
BCO is a significant problem of broilers, and is
almost certainly underdiagnosed. A detailed study
has shown that it accounts for losses in the region of
0.75% of all broiler placements
(
McNamee, 1998
)
.
This was estimated to cost the UK broiler industry 3
million per annum. The most common cause of
BCO, presently, is S. aureus, but other bacteria may
also cause the disease. S. aureus has been a difficult
pathogen to control in humans and cattle, where it
also causes significant problems. There have been
advances in the knowledge and understanding of fac-
tors contributing to infection and disease develop-
ment in chickens, which show that it should be possi-
ble, by good management practices and biosecurity,
to at least reduce the incidence of BCO. Develop-
ment of an effective vaccine would appear to be
some way off. It should be realized that since other
bacteria can cause the disease, a vaccine against S.
aureus will not totally prevent BCO. If other bacteria
can occupy the niche vacated by S. aureus, then the
incidence of BCO may not even be reduced; rather
different bacteria will be involved. The use of bacte-
rial interference in the prevention of BCO warrants
further investigation, and the availability of a disease
model using a natural route of infection will facilitate
such investigations .
266 P. T. McNamee & J. A. Smyth
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R

ESUM

E
Chondron ecrose bacterienne accompagn ee dune ost eomy elite
(n ecrose de la t ete du f emur) chez le poulet de chair
Une chondron ecrose bact erienne accompagn ee dune ost eomy elite
(BCO) a et e d ecrite chez le poulet pour la premi ` ere fois en 1972 et est
reconnue maintenant comme etant une cause importante de boiterie
chez le poulet de chair.
Des etudes r ecentes et syst ematiques des causes de boiterie chez les
poulets elev es en Irlande du Nord ont montr e que la BCO etait la cause
principale de boiterie en etant pr esente dans 17,3 % des cas chez les
oiseaux m ales. De plus la BCO a egalement et e d etect ee chez les
oiseaux 0trouv es morts0. Chez les m ales, les pertes totales dues ` a la
BCO ont et e estim ees ` a 0,75 % des oiseaux mis en place, qui en plus
de laspect bien- etre, repr esente une perte economique consid erable. La
maladie a et e observ ee chez les oiseaux ag es de 14 ` a 70 jours, mais
apparat la plupart des cas autour de 35 jours. Cette affection est
g en eralement due ` a Staphylococcus aureus, mais E. coli, des Staphylo-
coques coagulase-n egative et Enterococcus spp sont parfois impliqu es
et plus rarement dautres bact eries.
Les l esions sont plus g en eralement trouv ees associ ees aux plaques de
croissance des os longs, principalement la plaque de croissance
proximale du f emur et du tibiotarse, mais dautres os peuvent etre
affect es. Du fait que les l esions soient visibles ` a lil nu dans
seulement 40 ` a 67 % des cas, des examens histologiques sont
recommand es quand les l esions ne sont pas visibles ` a lil nu. Comme
les l esions peuvent etre pr esentes au niveau dune seule plaque de
croissance et du fait que les examens histologiques ne sont pas tr` es
souvent r ealis es, la BCO est tr` es certainement sous-diagnostiqu ee. La
pathog enie exacte nest pas connue, mais on pense que ladh erence des
bact eries du sang au niveau du cartilage et au contact des extr emit es des
vaisseaux sanguins est fondamentale.
Dans les conditions exp erimentales, les oiseaux infect es avec les
virus immunod epresseurs de lan emie infectieuse du poulet (CAV) et
de la maladie de Gumboro (IBDV) augmentent lincidence de la
maladie, alors quun rationnement de laliment r eduit lincidence de la
maladie. Les souches de S. aureus identiques ou presque aux souches
isol ees de cas spontan es de la maladie (d etermin ees par electrophor`ese
en champ puls e) ont et e celles isol ees ` a partir des duvets de couvoir et
` a partir des pr el` evements denvironnement des troupeaux de repro-
ducteurs, indiquant que linfection au niveau des elevages repro-
ducteurs et des couvoirs pouvait etre une source dinfection importante.
Il a egalement et e montr e que lhomme pouvait etre porteur de souches
de S. aureus sur les mains. Il y a une tr` es forte incidence de BCO chez
les oiseaux qui proviennent dufs pondus au sol. Ainsi lhygi ` ene et la
conduite de l elevage des reproducteurs et celle du couvoir peuvent
influencer lapparition de la maladie. Une bact eri emie est une condition
pr ealable pour la BCO. En effet, dans quelques troupeaux subissant des
pertes dues ` a la BCO, il y a aussi des pertes dues ` a une septic emie ` a
Staphylocoque. Ainsi, un traitement appropri e, appliqu e aux troupeaux
affect es devrait r eduire les pertes dues ` a la septic emie. Il devrait
egalement r eduire lapparition dune bact eri emie et le d eveloppement
de cas de BCO. Cependant, les oiseaux qui developpent d ej` a une BCO,
ne peuvent probablement pas r epondre au traitement. Le contr ole de La
BCO par vaccination ne semble probablement pas envisageable ` a court
terme. Des vaccins inactiv es nont pas et e efficaces et des recherches
compl ementaires sont n ecessaires pour identifier les facteurs de
virulence. Par ailleurs, plus dun type de bact eries est capable dinduire
la maladie. Une interf erence bact erienne a et e utilis ee avec succ` es chez
lhomme et la dinde pour contr oler les maladies ` a Staphylocoque et
justifie des etudes pour la pr evention de BCO chez le poulet. Ceci peut
avoir un avantage du fait que linterf erence bact erienne peut egalement
exclure certaines autres bact eries qui peuvent entraner la BCO. La
r ecente mise au point dun mod` ele exp erimental dans lequel S. aureus
est administr e par voie naturelle, permet la possibilit e d etudier
ult erieurement le r ole des facteurs pr edisposants et les strat egies
dintervention, incluant la vaccination et linterf erence bact erienne
dans la pr evention de la BCO.
Bacterial chondronecrosis in broilers 269
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ZUSAMMENFASSUNG
Bakterielle Chondronekrose mit Osteomyelitis bei Mastk uken in
Nordirland: Studien uber die

Atiologie, Pathogenese und


Bek ampfung
Die bakterielle Chondronekrose mit Osteomyelitis (BCO) bei H uhnern
wurde 1972 zuerst beschrieben und wird jetzt als eine bedeutende
Lahmheitsursache bei Mastk uken anerkannt. Neuere systematische
Untersuchungen uber die Ursachen der Lahmheit bei in Norirland
aufgezogenen Mastk uken ergaben, dass BCO bei 17,3% der lahmen
m annlichen Tiere vorlag und damit die h aufigste Lahmheitsursache
war. Auerdem wurde BCO bei Tieren festgestellt, die als 0tot
aufgefunden0 eingeliefert wurden. Die Gesamtverluste durch BCO bei
m annlichen Tieren wurden auf 0,75% aller eingestallten K uken
geschatzt, was zus atzlich zur Bedeutung f ur das Wohl der Tiere einen
betr achlichen wirtschaftlichen Verlust darstellt. Die Krankheit wurde
bei Tieren im Alter zwischen 14 und 70 Tagen festgestellt, doch die
meisten F alle traten im Alter um 35 Tage auf. Sie wird meistens durch
Staphylocccus aureus verursacht, aber manchmal sind E. coli, Koagu-
lase-negative Staphylokokken und Enterococcus spp. beteiligt und
selten andere Bakterien. Die L asionen wurden am h aufigsten im
Bereich der Epiphysenfugen der R ohrenknochen gefunden, vor allem
in der proximalen Epiphysenfuge des Femur und Tibiotarsus, aber
andere Knochen k onnen auch betroffen sein. Da die L asionen nur in
4067% der F alle mit dem bloen Auge zu erkennen waren, werden
histologische Untersuchungen empfohlen, wo makroskopisch keine
L asionen sichtbar sind. Da die L asion vielleicht nur in einer
Epiphysenfuge vorhanden ist und weil oft keine histologische Untersu-
chung durchgef uhrt wird, wird die BCO mit ziemlicher Sicherheit zu
selten diagnostiziert. Die exakte Pathogenese der Erkrankung ist
unbekannt, aber es wird angenommen, dass die Adh arenz von
h amatogenen Bakterien an exponierten Knorpel an den Enden der
Metaphysenblutgefae wesentlich ist. Unter kontrollierten Versuchsbe-
dingungen erh ohte die Infektion der Tiere mit den immunsuppressive n
Virusarten H uhneranamievirus (CAV) und Bursitisvirus (IBDV) die
H aufigkeit der Krankheit, w ahrend restriktive F utterung die Krankheit-
sh aufigkeit reduzierte. S. aureus-St amme, die mit Isolaten von
nat urlich vorkommenden Erkrankungsf allen identisch oder nahe mit
ihnen verwandt sind (wie mit der Pulsfeld-Gelelektrophorese festges-
tellt wurde), wurden aus Flaumresten in den Br utereien sowie aus der
Umgebung der Zuchtherden isoliert, was darauf hindeutet, dass
Infektionen in der Zuchtfarm und in der Br uterei eine wichtige
Infektionsquelle sein k onnten. Auerdem wurde nachgewiesen, dass
Menschen Gefl ugelst amme von S. aureus auf ihren H anden haben
k onnen. Bei K uken, die aus Bodeneiern geschl upft sind, gibt es eine
h ohere BCO-H aufigkeit. Somit k onnen die Hygiene-und Manage-
mentpraktiken in Zuchtfarmen und in der Br uterei das Vorkommen der
Krankheit beeinflussen. Bakteri amie ist eine Vorbedingung f ur BCO.
Tats achlich gibt es in manchen Best anden, die unter Verlusten durch
BCO leiden, auch Verluste durch eine Staphylokokken-Septik amie.
Somit sollte eine geeignete Behandlung erkrankter Best ande die
Verluste durch Septik amie reduzieren. Sie d urfte auch das Auftreten der
Bakteri amie und die Entwicklung von weiteren BCO-F allen redu-
zieren. Tiere, bei denen sich die BCO bereits entwickelt hat, reagieren
jedoch h ochstwahrscheinlich nicht auf die Behandlung. Die Bek amp-
fung der BCO durch Vakzinierung scheint auf kurze Sicht aussichtslos
zu sein. Einfache Bakterienimpfstoffe waren nicht wirksam, und viel
Grundlagenforschung ist notwendig, um die wichtigen Virulenzfakto-
ren zu identifizieren. Auerdem kann mehr als ein Bakterientyp die
Krankheit zu verursachen. Die bakterielle Interferenz ist bei Menschen
und Puten erfolgreich genutzt worden, um Staphylokokkenerkrankun -
gen zu verh uten, und berechtigt zu Untersuchungen im Hinblick auf die
Verh utung der BCO bei K uken. Das k onnte insofern n utzlich sein, als
das interferierende Bakterium vielleicht auch einige der anderen
Bakterien ausschliet, die BCO verursachen k onnen. Die k urzliche
Entwicklung eines Krankheitsmodells, bei dem S. aureus auf einem
nat urlichen Weg verabreicht wird, er offnet M oglichkeiten f ur die
weitere Untersuchung der Rolle von pr adisponierenden Faktoren und
f ur Interventionsstrategien zur Verh utung der BCO einschlielich
Vakzinierung und bakterieller Interferenz.
RESUMEN
Condronecrosis bacteriana con osteomielitis (necrosis de la
cabeza femoral) en pollos de engarde
La condronecrosis bacteriana con osteomielitis (BCO) en pollos fue
descrita por primera vez en el a no 1972 y en la actualidad es reconocida
como unacausa importante de cojera en pollos broiler. En estudios
recientes sobre causas de cojera en aves cradas en Irlanda del Norte se
demostr o que la BCO es la causa m as frecuente de cojera, estando
presente en un 17,3 de los pollos con cojera.Adem as, se detect o
tambi en en aves que aparecieron muertas.Las p erdidas totales de aves
macho debido a BCO se estimaron en un 0,75% del total de las aves
alojadas, hecho que adem as de afectar el bienestar, representa un
p erdida econ omica considerable. La enfermedad se ha observado en
aves de entre 14 y 70 das de edad, pero la mayora de casos aparecen
hacia los 35 das. La causa m as com un es Staphylococcus aureus, pero
E.coli, estafilococos coagulasa negativos y Enterococcus spp. tambi en
se encuentran ocasionalmente involucrados y, raramente, algunas otras
bacterias. Las lesiones se encuentran frecuentemente en los cartlagos
de crecimiento de los huesos largos,particularmente en el cartlago de
crecimiento del f emur y tibiotarso, pero tambi en se puden ver afectados
otros huesos. Se recomienda el examen histol ogico en el caso de no
observar lesiones macrosc opicamente, ya que, solamente en un
4067% de los casos se pueden observar lesiones macrosc opicas. Dado
que la lesi on puede estar presente en un solo cartlago de crecimiento y
que, con frecuencia, no se llevan a cabo estudioshistol ogicos, la BCO
es seguramente infradiagnosticada. La patog enesis exacta del proceso
es desconocida, pero parece fundamental la adherencia de una bacteria
de origen hemat ogeno al cartlago expuesto en los extremos de los
vasos sanguneos. Bajo condiciones experimentales, la infecci on de
aves con los virus immunosupresores de anemia infecciosa aviar
(CAV) y bursitis infecciosa (IBDV) incrementan la incidencia de la
enfermedad, mientras que las restricciones alimentarias disminuyen la
incidencia de la enfermedad. Se han aislado cepas de S.aureus id enticas
o muy relacionadas con cepas aisladas de casos naturales de la
enfermedad (mediante determinaci on por electroforesis de campo
pulsado), a partir de restos de plum on de incubadoras y tambi en del
ambiente de lotes de reproductores, hecho que indica que la infecci on
en las granjas de reproductoras y en las incubadoras podra ser una
fuente importante de infecci on. Tambi en se ha demostrado que las
personas pueden transportar cepas aviares de S.aureus en las manos. Se
observa una incidencia m as elevada de BCO en aves nacidas de huevos
puestos en el suelo. Por lo tanto, la higiene y las pr acticas de manejo en
granjas de reproductoras y en la incubadora puede influenciar la
aparici on de enfermedad. La bacteremia es unprerrequisito para que se
produzca la BCO. Adem as, en algunos lotes que padecen p erdidas
debido a BCO, hay tambi en p erdidas debidas a septicemias estafiloc o-
cicas. Por lo tanto, un tratamiento apropiado de los lotes afectados
debera reducir las p erdidas debidas a septicemia. Tambi en debera
reducir la aparici on de bacteremi a y el desarrollo de casos posteriores
de BCO. A un as, las aves en las cuales ya se ha desarrollado un
proceso de BCO, probablemente no responder an al tratamiento.
Actualmente, el control de la BCO mediante vacunaci on parece poco
probable. Las bacterinas simples no son efectivas y es necesaria m as
investigaci on b asica para identificar los factores de virulencia. Adem as,
la enfermedad puede ser causada por m as de un tipo de bacterias. La
interferencia bacteriana se ha utilizado con exito en humanos y pavos
para prevenir las enfermedades estafiloc ocicas y merece la investiga-
ci on para la prevenci on de la BCO en pollos. Esto puede representar
una ventaja ya que la bacteria que interfiere podra excluir otras
bacterias que causan la BCO. El reciente desarrollo de un modelo de
enfermedad en el cual S.aureus es inoculado por una va natural, es un
potencial para posteriores investigaciones del papel de factores
predisponentesy estrategias de intervenci on, includas vacunaciones e
interferencia bacteriana, para la prevenci on de BCO.
270 P. T. McNamee & J. A. Smyth
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