Diagnostic and Interventional Imaging (2012) 93, 351—359
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ICONOGRAPHIC REVIEW
Pitfalls in osteoarticular imaging: How to distinguish
bone infection from tumour?
a,∗ b c
T. Moser , M. Ehlinger , M. Chelli Bouaziz ,
c d d
M. Fethi Ladeb , J. Durckel , J.-C. Dosch
a
Department of Radiology, Notre-Dame Hospital, Montreal University Hospitals, 1560,
Sherbrooke Est, Montreal, Quebec H2T1H1, Canada
b
Department of Orthopaedic Surgery and Traumatology, Hautepierre Hospital, Strasbourg
University Hospitals, avenue Molière, 67098 Strasbourg cedex, France
c
Department of Radiology, Kassab Orthopaedic Institute, Ksar Said 2010, Tunisia
d
Department of Radiology 2, Hautepierre Hospital, Strasbourg University Hospitals, avenue
Molière, 67098 Strasbourg cedex, France
KEYWORDS Abstract In this article examining pitfalls in osteoarticular imaging we examine the diffe-
Bone infection; rential diagnosis of osteomyelitis from bone tumours. We describe the different features which
Osteomyelitis; differentiate these two types of disease in radiology and CT and MRI scanning.
Bone tumour; © 2012 Éditions françaises de radiologie. Published by Elsevier Masson SAS. All rights reserved. Sarcoma;
MRI
The appearances of bone infection and bone tumour are often similar on imaging. The
differential diagnosis of osteoarticular infection includes above all malignant tumours but
also some benign, inflammatory tumours (osteoid osteoma osteoblastoma) and pseudo-
tumours (eosinophilic granuloma). The clinical and laboratory context does not always
discriminate between these and the diagnosis is occasionally only obtained on histological
examination. This confusion can lead to delays in treatment and inadequate management.
We describe here the imaging appearances of osteomyelitis, specifically those of sub-
acute osteomyelitis. It is estimated that 50% of cases in children are initially confused with
tumour [1].
∗
Corresponding author.
E-mail address: [email protected] (T. Moser).
2211-5684/$ — see front matter © 2012 Éditions françaises de radiologie. Published by Elsevier Masson SAS. All rights reserved. doi:10.1016/j.diii.2012.01.021
352 T. Moser et al.
Definitions Radiological signs
Three pathways of infection of bone by pathogenic orga- The radiological signs of osteomyelitis involve a variable
nisms can be distinguished: haematogenous, direct (after combination of trabecular and then cortical osteolysis with
trauma or surgery) or contiguous infection (joint or soft tis- sequestrum, a periosteal reaction and soft tissue abnorma-
sue infection). The term osteomyelitis is usually reserved lities (collections, fistulae).
for bone infection due to haematogenous spread (centrifu-
gal extension). Osteitis is a generic term combining bone Osteolysis
infections with a breach in the bone cortex from the outset
Osteomyelitis preferentially affects the metaphyses and epi-
(centripetal extension). Septic osteoarthritis is a combina-
physes of lower limb, long bones. Osteolysis is due to the
tion of septic arthritis with co-existent bone infection [2].
inflammatory reaction and septic necrosis in the bone layers.
Acute, sub-acute and chronic osteomyelitis can be con-
It is characterised initially by a zone of bone demineralisa-
sidered separately. The criteria for length of infection
tion with blurred edges (Fig. 1), and then extends to the
(acute = less than one month, sub-acute = one to three
cortex, taking on a moth-eaten or porous appearance. These
months, chronic = more than three months) are arbitrary and
are types IC, II and III of the Lodwick classification [10]. Tra-
vary according to the author. Histologically, acute infection
becular and cortical osteolysis can be examined in far more
is suppurative and not contained; sub-acute infection is sup-
detail by CT scanning. This can show a non-specific increase
purative and contained (abscess) whereas chronic infection
in bone marrow density due to the inflammatory infiltrate
is variably suppurative and associated with healing bone
[7]. Finally, the occasional presence of gas (Fig. 2) or fat-
remodelling [2].
fluid levels in the bone marrow cavity is very specific for
osteomyelitis outside of a context of trauma [11,12].
Clinical and laboratory features
Periosteal reaction
A periosteal reaction is present in more than 50% of cases of
Acute osteomyelitis is found predominantly in children and
acute, sub-acute or chronic osteomyelitis. It usually occurs
classically presents as pain, features of infection, local
earlier and is more clearly visible in children who have an
swelling and loss of function. It is usual to find an acute
active periosteum, which is poorly adherent to bone. It
phase reaction with leukocytosis and raised C-reactive pro-
needs to be ossified in order to be visible (Fig. 3), although
tein. Blood cultures are positive in almost half of cases. The
can be seen more early on CT scanning than by radiographs.
organism most often isolated is Staphylococcus aureus (in
The periosteal reaction can be unilamellar, plurilamel-
90% of cases).
lar (‘‘onion skin’’) or compact. It is relatively non-specific
These signs are not specific as they can be present in some
and has many causes: physiological (premature infants),
pseudotumours and inflammatory tumours such as Ewing’s
fracture, osteosarcoma or eosinophilic granuloma for a unil-
sarcoma [3]. They are often absent or less pronounced
amellar periosteal reaction, Ewing’s sarcoma or osteosar-
in sub-acute or chronic osteomyelitis and in infants. The
coma for a plurilamellar reaction and fracture or osteoid
diagnosis is particularly difficult in a non-febrile child in a
osteoma for a compact periosteal reaction. A spiculated
context of injury [4].
Radiographic and CT scan appearances
Radiographs are always essential in the acute phase [5],
although offer poor sensitivity, in the region of 37% with
a specificity of 73% in the study by Tumeh et al. [6]. CT
scans are particularly useful in the sub-acute or chronic
phase [7].
Chronology of radiological changes
Initially, radiographs are normal. They may then show suc-
cessive swelling of the soft tissues (early), bone demine-
ralisation (after seven days), a periosteal reaction (after
15 days), and trabecular and cortical osteolysis (after three
weeks) [8].
The duration of an infection is an important factor where
this can be assessed reliably from repeated films. Rather
schematically according to Greenspan [9], Ewing’s sarcoma
requires approximately four to six months, osteomyeli-
tis four to six weeks and eosinophilic granuloma only
around ten days to produce the same amount of bone Figure 1. Heterogeneous demineralisation in acute humeral
destruction. metaphyseal osteomyelitis.
Pitfalls in osteoarticular imaging: How to distinguish bone infection from tumour? 353
Figure 2. Gas present in the bone marrow cavity indicating reac- Figure 4. Sequestrum appearance in sub-acute tibial osteomyeli-
tivation of chronic osteomyelitis. tis. Note also the bone reaction which surrounds the focus of
infection (‘‘involucrum’’).
zone (Fig. 4). It is important to diagnose as it is firstly very
suggestive of infection and secondly represents a reservoir
of organisms, which are not readily accessible to antibiotics,
and often requires surgical excision. The sensitivity of this
sign to diagnose infection is poor with radiographs but better
for CT scans [6,7]. It is not entirely specific as it is also seen
in eosinophilic granuloma, fibrosarcoma and can occasio-
nally be confused with a calcified nidus of osteoid osteoma
[14].
Soft tissue abnormalities
The fatty planes, which are visible on radiography are clas-
sically abolished by infection and displaced by tumours.
Collections and fistulae are invisible on radiography unless
fistulography is performed. The first line investigation to
examine a subperiosteal or juxta-osseous collection is ultra-
sound. Bone and soft tissues can be studied in great detail
by MRI. Failing this, a CT scan with contrast injection and
multi-planar reconstructions can be used for a rapid urgent
patient assessments [15].
Soft tissues calcifications or ossifications are rare in
osteoarticular infection due to the classic pyogenic orga-
nisms and are more suggestive of a neoplastic (osteosar-
coma) or pseudo-neoplastic (circumscribed myositis ossifi-
Figure 3. Compact periosteal reaction associated with sub-acute
cans) process. On the other hand it is a characteristic finding
tibial osteomyelitis.
in tuberculosis and is also seen in hydatid disease and fungal
infections.
periosteal reaction with a Codman spur suggests osteosar-
coma or Ewing’s sarcoma [13]. Clinical-radiological features and differential diagnosis Sequestrum
Acute osteomyelitis
Sequestrum is a fragment of dead bone surrounded by gra-
nulation tissue and is seen in more than fifty per cent of The diagnosis is suggested from clinical evidence (infection,
cases of chronic osteomyelitis. It appears on radiographs as metaphyseal pain) and laboratory findings (acute inflamma-
a dense, often irregular fragment with a surrounding clear tory reaction, positive blood cultures). Initial radiography
354 T. Moser et al.
is normal. Ultrasound can be used to investigate for sub- cortical bone. The most classical form of this is the Brodie
periosteal abscesses and guide aspiration puncture [18]. The abscess (Fig. 5) [16]. This is usually found in the metaphy-
initial changes in bone marrow signal can only be seen on MRI sis and may extend to the epiphysis along the epiphyseal
(see below). cartilage. It is usually 1 to 5 cm in diameter and is ovoid
or funicular along the long axis of the bone. A periosteal
reaction or appearances of sequestrum are typically absent.
Sub-acute osteomyelitis
Diaphyseal forms of disease have been described to have
This is the most difficult situation, which raises the problem
far more variable appearances which may include cortical
of the differential diagnosis from tumour. We propose that
thickening or a periosteal reaction and contains sequestrum
the Gledhill and Rombouts classification [16,19] be used as
[17]. The main differential diagnoses are eosinophilic granu-
the basis for description.Type 1 refers to the appearances
loma and osteoid osteoma (Fig. 6).Type 2 refers to a zone of
of a single osteolytic lesion, which may or may not be sur-
metaphyseal osteolysis with cortical destruction. The main
rounded by a reactive bony reconsolidation line which spares
Figure 5. Brodie’s abscess of the radial metaphysic (type 1 sub-acute osteomyelitis). Note the epiphyseal extension through the growth
cartilage, which is far easier seen on CT.
Figure 6. Sub-acute tibial osteomyelitis (type 3 sub-acute osteomyelitis). Osteoid osteoma and stress fractures can be excluded by a CT scan.
Pitfalls in osteoarticular imaging: How to distinguish bone infection from tumour? 355
Figure 7. Brodie’s abscess of the femoral head (type 1 sub-acute
osteomyelitis). The presence of bony sequestrum is atypical and
raises the possibility of osteoid osteoma.
differential diagnoses are osteosarcoma and an aneurysmal
cyst.Type 3 involves thickening of the diaphyseal cortex
caused by a compact periosteal and an endosteal reac- Figure 8. Plurilamellar femoral periosteal reaction (type 4 sub-
tion. The differential diagnosis includes osteoid osteoma acute osteomyelitis). The differential diagnosis is Ewing’s sarcoma.
(Fig. 7) and fatigue fractures or stress reactions. CT scans
are very useful to look for abnormalities which are not
Chronic suppuration may be present, the classical compli-
visible on radiographs.Type 4 refers to a plurilamellar dia-
cation of which, which is seen in 1% of cases, is squamous
physeal periosteal reaction. The main differential diagnosis
cell carcinoma developing from epithelial metaplasia in the
is Ewing’s sarcoma (Fig. 8).
sinus tract [22].
Other forms exist including epiphyseal disease imita-
ting chondroblastoma or a giant cell tumour (Fig. 9) [20]
and ‘‘metaphyseal equivalent’’ forms which affects the flat
MRI appearances
bones (ilium) or short bones (calcaneum, vertebra) immedi-
ately next to the epiphyseal cartilage [21].
MRI is extremely useful for early diagnosis of acute
osteomyelitis with sensitivities and specificities of between
Chronic osteomyelitis
60 and 100% depending on the study. The lowest values
Healing bone changes predominate in the chronic stage of were obtained from studies performed without injection
osteomyelitis and episodes of reactivation are common. of contrast medium whereas values of over 90% have
Figure 9. Sub-acute osteomyelitis of the femoral head. The differential diagnosis is giant cell tumour.
356 T. Moser et al.
been achieved from the most recent work. MRI was and bone healing. The trabecular bone signal abnormalities
previously performed second line after bone scintigra- in acute osteomyelitis are homogeneous, poorly delineated,
phy and is now performed directly after radiographs and low or normal intensity on T1 and increased intensity on T2
ultrasound. (oedema), simultaneously involving the bone marrow cav-
ity, cortical bone and the adjacent soft tissues. The signal
abnormalities are better delineated, greatly reduced inten-
MRI signs sity on T1 and increased intensity on T2 (collection) in
sub-acute osteomyelitis, occasionally with reduced intensity
sequestrum on T1 and T2 (Fig. 10). Signal abnormalities in
Abnormal bone marrow signal
chronic osteomyelitis are heterogeneous and involve a com-
Abnormalities in bone marrow signal are initially due to the
bination of reduced intensity T1 and increased intensity T2
oedema, exsudate, the presence of inflammatory cells and
areas and reduced intensity T1 and T2 areas (sclerosis) [23].
bone ischemia and then reflect the formation of collections
Figure 10. a: weighted T2 MRI appearances of sequestrum and b: periosteal reaction correlated with CT scan findings.
Figure 11. Acute osteomyelitis of the humeral metaphysic (same patient as in Fig. 1). The necrosis and early intra-osseous collection are
clearly seen after injection of contrast medium (a). On the T1-weighted sequence (b), fat can be seen in the focus of osteomyelitis.
Pitfalls in osteoarticular imaging: How to distinguish bone infection from tumour? 357
The periphery of the bone collections can be highlighted by or any other organ) and appears to be due to the pres-
injecting contrast medium, making them easier to detect ence of paramagnetic free radicals produced by activated
(Fig. 11) [24]. macrophages. The penumbra sign is more apparent when
The signal abnormalities seen with oedema are a sensi- the granulation tissue is young and represents direct annu-
tive but relatively non-specific sign of osteomyelitis. Some lar uptake of contrast. It appears to be very specific (99%)
signs which are variably present are more specific for the for abscess although its sensitivity varies from 27% to 75%
diagnosis. depending on the study [28,29].
The double line sign described on T2-weighted sequences
Fat globules (acute osteomyelitis) is less useful. It represents the internal ring (increased
intensity) and external ring (reduced intensity). Its visibility
Acute osteomyelitis causes septic necrosis of the bone mar-
depends on the window used and offers a sensitivity of only
row, releasing fat particles which sediment with pus to form
22% [28].
fat-fluid levels inside or outside of the bone [12]. The pres-
ence of fat in soft tissues (Fig. 12) is believed to be due
to the fat passing through the Haversian canals and is an
Periosteal reaction and sequestra
indirect sign of a breach in cortical bone [25].
The periosteal reaction is often missed on MRI although it
Davies et al. [26] have studied the presence of fat
can be seen before ossification and therefore earlier than
in a focus of osteomyelitis. This sign is found in acute
on a CT scan. The target appearance on a T2-weighted
osteomyelitis (Fig. 11) and is due either to persistent normal
sequence (Fig. 14) represents the periosteal lamellae sepa-
bone marrow within the oedema or to linear or to globular
rated by granulation tissue [30]. The sequestra appear as
clumps of necrotic bone marrow.
reduced intensities on all sequences.
Penumbra sign (Brodie’s abscess)
Soft tissue abnormalities
The target appearance of the Brodie’s abscess on MRI was
initially described by Marti-Bonmati et al. [27]. Four con- Sequences with contrast medium injection and abolition of
centric layers are seen: the centre (pus) which is reduced in the fat signal or useful to delineate collections and fistula
intensity on T1 and increased intensity on T2, the internal tracts within inflammatory changes [31].
ring (abscess wall) which is of normal intensity on T1 and
increased intensity on T2, the external ring (reactive scle-
Texture sign (soft tissue mass)
rosis) which is reduced in intensity on T1 and T2 and the
periphery (bone oedema) which is reduced in intensity on It is not always easy to distinguish between inflammatory or
T1 and increased on T2. neoplastic changes in a soft tissue mass. Classically, inflam-
The penumbra sign (Fig. 13) described on T1-weighted mation is diffuse and crosses the fascias whereas tumour
sequences represents the internal ring which has a rela- forms a well defined mass which preserves the fascia. The
tively high density signal compared to the other layers of texture sign proposed for use in following up treated sar-
the target. Histologically, this represents the granulation tis- comas can also be used. A visible muscular framework in a
sue surrounding all abscess cavities (in bone, soft tissues T1-weighted sequence supports inflammatory changes when
Figure 12. Fat present in soft tissues confirming the diagnosis of sub-acute osteomyelitis in a bone lesion with soft tissue mass. The
presence of sequestrum (b) is also suggestive.
358 T. Moser et al.
Figure 13. Penumbra sign in a Brodie’s abscess centred on the tibial physis. On the T1-weightedsequences (a), an internal reduced
intensity ring is silhouetted by the contents of the abscess on one side by the external ring of sclerosis and on the other by bony oedema.
After injection of contrast medium and abolishing the fat signal (b), the internal ring representing the granulation tissue picks up contrast
medium intensely.
attention to the aggressive presentation of benign inflam-
matory bone tumours (osteoid osteoma, osteoblastoma and
chondroblastoma), eosinophilic granuloma and stress frac-
tures which cause bone and soft tissue oedema that is often
disproportionate to the size of the lesion [33]. In these situa-
tions, careful examination of radiographs is essential and a
scan targeted on the abnormal area can occasionally reveal
subtle abnormalities (nidus, fracture line, stress reaction).
The differential diagnosis between osteomyelitis and
bone oedema as a reaction to neighbouring septic arthri-
tis or cellulitis is also difficult. Bone would appear to take
up contrast medium less intensely than soft tissue in cel-
lulitis with reactive bony oedema, whereas contrast uptake
appears to be equivalent in osteomyelitis [24]. Bone oedema
as a reaction to septic arthritis appears to be less intense on
T1 sequences than in osteomyelitis [34].
An additional approach may be to use a contrast
media containing supermagnetic iron particles (SPIO) which
shorten the T1 and particularly T2 relaxation time. After
intravenous injection these particles are taken up by the
reticulo-endothelial cells and accumulate in macrophages
and fibroblasts in the inflamed area. These contrast media
Figure 14. Appearances of a periosteal reaction on a T2-weighted
could help to delineate inflammatory reactions and distin-
MRI sequence. The unilamellar periosteal reaction and reduced
guish them from neoplastic disease [35,36].
intensity bone cortex are separated by increased intensity gra-
nulation tissue.
signal abnormalities are present on a T1-weighted sequence Disclosure of interest
[32].
TM is a consultant for Arthrovision.
Differential diagnosis by MRI
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