365
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Pictorial
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Bacterial Osteomyelitis: MR, and Scintigraphy Richard
H. Gold,1
Randall
A. Hawkins,1
Findings and Robert
osteomyelitis
and correlate these imaging
from
the changes methods.
cellulitis.
In this
of bacterial
article,
osteomyelitis
we
on Plain Radiography,
CT,
of bone
of pen-
D. Katz2
Early detection of osteomyelitis is essential if appropriate therapy is to be started before bone devitalization. Although the “Tc-methyIene diphosphonate (MDP) bone scan may signify the possibility of osteomyelitis days or weeks before osseous changes are apparent on standard radiographs, the radiographic changes may provide important diagnostic clues. The 67Ga-citrate scan augments the diagnostic value of the “Tc-MDP scan, and the 1111n-labeled WBC scan is useful for detecting abscesses. CT aids in the detection of sequestra, and MR imaging is useful in defining the extent of the inflammatory process and in distinguishing
Essay
ment
become
sequestrated,
osteal new bone, or involucrum,
a thick
may surround
sheath
it. The infection
review
shown
by
Advances in imaging patients with bacterial osteomyelitis have improved the prognosis of the disease. In this article, we review and correlate the changes of bacterial osteomyelitis shown by various methods of imaging.
Plain Radiography Because myelitis
the clinical course
is rapid,
of acute hematogenous
early detection
is essential
osteo-
if therapy
is to be
started before bone devitalization. Although changes on plain films occur relatively late in comparison with scintigraphic changes, plain radiography usually is the initial imaging examination and may provide important clues, such as the appearance of periosteal new bone (Fig. 1) and widening of the joint (Fig. 2). In infants, the presence of excess
sonography joint fluid,
is useful in confirming that, if drained early,
obviates vascular tamponade and resultant osteonecrosis of the epiphysis. In childhood, the vascular metaphysis is the usual site of infection. After infancy, the physis prevents the spread of infection to the epiphysis (Fig. 3). Should the spaceoccupying
exudate
increase
the
intramedullary
pressure
and
strip the peniosteum, vascular thrombosis is followed by bone necrosis and formation of sequestra. Should an entire segReceived January 15, 1991 ; accepted I
Department
A. H. Gold. 2 Department AJR 157:365-370,
of Radiological
Sciences,
after revision March 1 1 , 1991. University
of California,
School
of Medicine,
Fig. 1.-Anteroposterior myelitis vs malignancy. A, Acute hematogenous 7-year-old boy. Destructive
activated
by benign
1991 0361-803x/91/1572-0365
C American
Roentgen
show
staphylococcal changes are
penosteal
new
bone:
osteo-
osteomyelitis of humerus in a present in metaphysis. When
stimuli such as pus, blood, or edema,
the inner layer
of displaced periosteum produces uninterrupted new bone of uniform density. B, Ewing sarcoma of humerus in 18-year-old man. Periosteal new bone stimulated by undenying malignancy tends to be interrupted and not uniform, and may exhibit multiple delicate longitudinal layers or perpendicular spicules. The latter are reflected in fuzzy-appearing margins of mid shaft. Longitudinal layers (“onion skinning”) terminate in Codman triangles (arrows), which commonly occur in association with Ewing sarcoma, but are uncommon with benign disease.
1 0833
Le Conte
Ave.,
of Radiology, Beverly Hills Medical Center, 1177 5. Beverly Dr., Los Angeles, CA 90035. August
radiographs
Ray Society
Los Angeles,
CA 90024.
Address
reprint
requests
to
are foci for continued are
essential.
small
sequestra.
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infections
infection,
Tomography Ring
(Fig.
their
detection
and excision
CT may be required
or sequestra
may
to detect
complicate
pin-tract
4) [1].
The onset of subacute hematogenous osteomyelitis (Brodie abscess) is insidious, and systemic manifestations are mild on absent (Fig. 5) [2]. Chronic osteomylitis results when there is continuation
which
of the
leads
inflammatory
to sclerosis
Disorders associated with include chronic granulomatous
deficiency 6),
bacterial
urinary
In contrast
of hematogenous
osteomyelitis
of
leading to an increase in articular interspace. This phenomenon is uncommon In more constrained joints of adufts. In infancy, transphyseal blood vessels may transmit infection from metaphysis to epiphysis, with secondary Involvement of joint. A widened joint is obvious in this patient, as are destruction of humeral head and exuberant uniform periosteal new bone.
may perforate the involucrum in the form of a cloaca, leading to soft-tissue abscesses and sinus tracts. Because sequestra
years,
multifocal disease
bacterial osteomyelitis of childhood, immune
on vascular
catheters
and immunosup-
therapy. to nontuberculous
tuberculous
radiograph
many
disorders, sickle cell anemia and its variants (Fig. abuse (Fig. 7), diabetes mellitus, and subacute endocarditis. Other predisposing factors are long-
indwelling
pressive
Fig. 2.-Anteroposterior
over
IV drug
term
humerus in a 10-month-old girl. In infants and children, osteomyelitis near end of a bone may cause joint to fill with a sympathetic effusion or exudate,
process
and deformity.
osteomyelitis
osteomyelitis
has
a more
of the
insidious
spine,
onset
and
progression, and produces greater destruction and anterior wedging of the vertebral bodies. Tuberculous infection produces the larger soft-tissue (“cold”) abscess (Fig. 8A). Tuberculosis of the spine may give rise to the aneurysmal syndrome (Fig. 8B) and calcific debris. Joint tuberculosis, unlike pyogenic infection, progresses very slowly, and is associated with the diagnostic
triad
of Phemister
tends toward multifocality bular bones (Fig. i 0).
(Fig.
and
9). Tuberculosis
involvement
in children
of the short
tu-
CT and MR Imaging MR imaging
is superior
to CT for evaluating
the extent
of
I Fig. 3.-Tomograms show effect of physis as a barrier to spread of infection. A, Staphylococcal osteomyelitis of femur in a 12-year-old girl. Serpentine foci of osteolysis in metaphysis and diaphysis represent abscess cavities. Disappearance of transphyseal blood vessels after infancy has allowed physis to prevent spread of infection to epiphysis. B, Tuberculosis of the femur in a 7-year-old breached by tuberculous infection. Alternatively,
might have spread to epiphysis
boy. As shown here, physis of older children since metaphysis of hip joint is intracapsular,
by way of joint itself.
is frequently
the infection
Fig. 4.-Radiograph shows ring sequestrum of pin-tract osteomyelitis complicating skeletal fixation of tibial fractures in a 25-year-old man. Diagnostic of a major pin-tract infection, necrotic ring of sclerotic bone (arrow) is separated from surrounding viable bone by exudate or granulation tissue. It is easily distinguished from clinically insignificant thermal osteonecrosis caused by high-speed drilling of a pinhole, which is characterized by a broad zone of sclerosis around the pin tract, but not by a separated ring; nor should it be confused with fluffy reparative bone in tract seen after pin removal.
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1
Fig.
5.-Brodie
radiograph
abscess
in distal
tibia
shows sharply marginated
of a 16-year-old
cavity. Sometimes
girl. cavity present,
Oblique is surmay be
rounded by sclerosis. Soft-tissue swelling, while usually absent. Sequestra are uncommon and periosteal new bone inconspicuous (arrow). Abscess is characteristically found in lower tibial metaphysis in children and adolescents, and metaphysis or diaphysis of femur or tibia in adults. Staphylococcus aureus is the usual cause.
infection.
CT
is superior
to
MA
imaging
for
detection
Fig. 6.-Anteroposterior radiograph shows changes of salmonellal Osteomyelitis in tibias of a 3-year-old giri with sickle cell anemia. Susceptibility to hematogenous osteomyelitis is increased manyfold in patients with sickle cell anemia and related disorders. Approximately 50% of cases are caused by Salmonella. Osteomyelitis may occur within a region that has been previously devitalized by infarction. As in this case, multiple bones are frequentiy affected and lesions may be bilaterally symmetric. Thick and occasionally layered periosteal new bone (arrows) and longitudinal intracortical fissures may parallel extent of lesion. These findings, however, are not specific for osteomyelitis, and may accompany infarction alone.
of
and cloacae and can also depict intraosseous gas, an infrequent but reliable sign of osteomyelitis. However, in a collapsed vertebral body, a linear streak of gas sequestra
(Fig.
1i )
merely signifies an intraosseous vacuum resulting from posttraumatic osteonecrosis (KUmmell disease). MR imaging aids in planning surgery by delineating sinus tracts and soft-tissue
abscesses, by differentiating osteomyelitis by disclosing the extent of intramedullary
from cellulitis, and involvement. MR is particularly helpful in the evaluation of the diabetic foot (Fig. 1 2) [3]. MA should be used only when it might provide information
unavailable
from less expensive
imaging
methods
and when the results might affect management significantly. For evaluation of osteomyelitis, MR is as specific as or more specific
and more
sensitive
ylene diphosphonate
than the three-phase
9Tc-meth-
(MDP) bone scan (Fig. 13). The specific-
ity of MR is increased
by plain
radiographic
correlation
and
by obtaining both Ti and T2-weighted images. The edema and exudate of active infection have a low-intensity signal on Ti-weighted images and a high-intensity signal on T2weighted images. -
Fig. 7.-Pseudomonas infection of left stemoclavicular joint in a 30year-old male heroin addict. Anteroposterior tomogram shows erosions and joint widening. An increased frequency of infection in IV drug abusers results from hematogenous spread from contaminated hypodermic needles. Spine, sacrolliacjolnt, stemoclavicularjoint, and symphysis pubis, sites most commonly Involved in order of decreasing prevalence, represent the four S’s of osteomyelitis associated with IV drug abuse. In some series, Gram-negative organisms such as Pseudomonas and Kiebsiella have prodominated, while in others most frequently cultured.
Staphylococcus
“flow”
images,
aureus
has been
the organism
Scintigraphy Aadionuclide studies pected osteomyelitis beled WBC scan, and bone scan may signify weeks
before
radiographs.
osseous “Tc-MDP
useful in examining patients with susinclude the 99mTc-MDP scan, 1In-la67Ga-citrate scan [4]. The mTcMDP the possibility of osteomyelitis days or changes bone
are scans
apparent are
sensitive
on
standard indicators
of altered osteoblastic activity, but local disturbances in vascular perfusion, clearance rate, permeability, and chemical binding also affect imaging. On standard 99mTc-MDP scans it sometimes may be difficult to differentiate soft-tissue uptake from bone uptake in patients with known cellulitis and possible underlying
osteomyelitis.
phase “Tc-MDP
To address
scan was developed,
this problem,
consisting
the three-
of dynamic
or “angiogram”
5-hr delayed initially high
blood-pool
images,
and 2- to
images (Fig. i 3). Cellulitis is characterized by an soft-tissue uptake in the flow phase, and pro-
gressively lower uptake compared with bone uptake in later phases. In contradistinction, osteomyelitis gives rise to progressively increasing bone uptake over the course of the study. The combination of cellulitis and osteomyelitis produces increased bone and soft-tissue uptake in all three phases.
The 99mTc-MDP
scan is not specific
for osteomyelitis,
and in the appropriate
clinical setting
may suggest
conclusively
the diagnosis.
A fourth
establish
24 hr after infection) results
may be useful in patients
at the end of three
phases,
phase
but cannot (imaging
with equivocal
as osteomyelitis
usually
368
GOLD
ET
AL.
AJR:157,
Fig. 8.-Tuberculosis
August
1991
of spine.
A, CT scan shows erosion of right ilium by a
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cold iliopsoas abscess that extended from spine to pelvis. Patient was a 23-year-old man with a 7-month history of pain and weakness of right lower limb. B, Lateral radiograph of lumber spine in a 45-
year-old man shows aneurysmal
syndrome due
to tuberculosis. Although narrowing of intervertebral disk usually is earliest radiographic feature of both nontuberculous and tuberculous osteomyelitis, scalloping of anterior (and sometimes lateral) margin (arrows) of vertebral bodies (aneurysmal syndrome) is associated only with tuberculous infection. Aneurysmal syndrome is so-called because concavities simulate those caused by transmitted pulsations of an aortic
aneurysm. Scalloped vertebrae 5005$ cavity.
lie within an ab-
Fig. 9.-Anteroposterior radiograph of tuberculosis ofthe kneeln a 46-year-old man. Tending to have a more insidious onset than nontuberculous septic arthritis, tuberculous arthritis is also associated with profound osteoporosis, marginal erosions, and long-standing
preserva-
tion of contacting articular nostic triad of Phemister.
the diagin sub-
chondral
bone of tibia
tuberculous
cartilage, Rarefactions
reflect
undermining
by
pannus.
Fig. 10.-Radiograph
of tuberculous
dactylitis
in a 1-year-old boy. In children, tuberculosis has a tendency toward multifocality and involvement of short
tubular
dactylitis, tends
bones.
unlike
Lesion
tuberculosis
not to invade
adjacent
of tuberculous bones, joints. In proximal
of long
phalanx of index finger, shown here, slow daboration of periosteal new bone that accompanied gradual resorption of inner surface of cortex led to a typically expanded fusiform appearance called spina ventosa (literally, a wind-filled projection, such as a finger).
Fig. 11.-Chronic trum
of proximal
osteomyelitis tibia.
Six years
with sequesearlier,
this 30-
year-old
man had a fracture of distal tibia that became infected after fixation with an intramedullary rod. Rod was subsequentiy removed. Cur-
rent bone
radiographs disclosed sclerotic reactive outlining track of former rod. Corresponding “Tc-MDP bone scan revealed striking increase in activity in proximal tibia. A, CT scan of proximal tibia shows rod track
surrounded by a thick, sclerotic rim and containIng a central sequestrum. Adjacent marrow appears normal. B, Axial MR image (SE 1500/56) shows a bright, high-intensity abscess in rod track, with a central low-intensity sequestrum and a rim of low-intensity sclerotic bone. These findings, together
with
absence
of high signal
intensity
in
adjacent marrow and soft tissues, Imply that active infection is present only in rod track.
provokes
further
increase in activity. Single-photon emission additional anatomic information. Although the overall sensitivity of the 99mTc-MDP scan for active osteomyelitis is high (approximately 95%), false-negaCT bone scans provide
tive diagnoses
may occur,
particularly
in neonates.
Both
the
1111n-labeled WBC scan and the 67Ga scan are useful adjuncts, and while usually no more sensitive than the combination of Tc-MDP
bone
scans
and
plain
radiographs
in detecting
osteomyelitis, they are more specific (Figs. 14 and 15). The 111In-WBC scan, although positive in some noninfected frac-
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Fig. 12.-Differential
diagnosis
in this 84-year-old
diabetic
woman
includes
neuropathic
osteoarthropathy,
cellulitis,
pyarthrosis,
and osteomyelitis.
A, Anteroposterior radiograph of foot shows striking osteoporosis and possible erosion of medial margin of head of second metatarsal. Results of three-phase Tc-MDP bone scan were equivocal. B and C, Ti-weighted (SE 500/28, B) and T2-weighted (SE 1500/56, C) coronal MR images show normal signal intensity in bones and joints adjacent to clinically suspicious areas, thereby excluding Soft tissues medial to first metatarsophalangeal weighted image, consistent with cellulitis.
osteomyelitis and pyarthrosis. Neuropathic osteoarthropathy is also unlikely in absence of joint eftusions. joint (arrows) have decreased signal intensity on Ti-weighted image and increased intensity on T2-
i. E1
‘
1 s.’-
B
Fig. 13.-Acute
hematogenous
osteomyelitis
of lumbar
C
spine
in a 59-year-old
man, proved
by biopsy.
Comparison
of imaging
techniques.
A, Lateral radiograph shows narrowing of L3-L4 disk, osteolytic foci next to endplates, and erosion of superior endplate of L4 (arrow). B and C, Three-phase “Tc-MDP bone scan shows a corresponding gradual increase in activity in dynamic flow phase (B), which becomes intense on 5-hr postinjection image (C).
even
more
0, PET scan in coronal plane, performed as part of an investigational study approved by the Human Subjects Protection Committee, shows a corresponding mild increase in activity (arrow) due to a focus of leukocytes preferentially metabolizing glucose from lV-infused FDG. E, TI-weighted sagittal MR image (SE 500/28) shows relatively high-intensity fatty marrow has been replaced by edema of intermediate intensity in bodies of L4 and L5, and adjacent endplates have undergone central destruction. F, T2-weighted sagittal image (SE 2000/84) shows involved vertebrae have a high-intensity signal. An even more intense focus centered at intervertebral
disk represents
an abscess.
370
GOLD
ET AL.
AJR:157,
August
1991
...‘, I,.
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:
#{149} -#{149}-
F”..
: ./
. t
24H .
A
;.
B
Fig. 14.-Usefulness of sequential ‘“Tc-MDP and 7Ga scans in evaluating suspected chronic osteomyelitis. Eleven years earlier, a 34-year-old man had a fracture of the right femur that was stabilized with an intramedullary rod. One year later, fracture healed and rod was removed. Since then, he had had intermittent thigh discomfort that had increased during the past 6 months. New radiographs disclosed diffuse cortical thickening and mottled sclerosis of middle third of
femur. A, A ‘“Tc-MDP four-phase scan shows progressively increasing bone and soft-tissue activity throughout flow, blood-pool, and 4-hr phases, culminating in strikingly increased activity in femoral shaft on this 24-hr delayed image. B, Additional evidence of chronic osteomyelitis, as well as a soft-tissue abscess, is provided by a ‘VGa scan showing focus of intense activity extending from medial soft tissues (arrow) to femur.
tunes, still tends to be preferred over the 67Ga scan because of its greater specificity for infection. The sensitivity of the 111In-WBC scan is greater for acute than for chronic infection, whereas the 67Ga scan is equally sensitive for both. Positron
emission
the skeletal like
system
e9mTcMDP,
blastic
tomography
by using
is taken
activity
and
local
(PET)
IV-infused
up by bone
vascular
produces
fluorine-i
in proportion
and
physical
images
of
use
of
2-[18F]-fluoro-2-deoxy-D-glucose
the specificity
may yield an abnormal
of PET. finding
Osteomyelitis
on PET body
nevertheless scans
(Fig. 13).
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1 . Nguyen
to osteo-
1986;158:129-131 2. Miller WB Jr, Murphy WA, Gilula LA. Brodie abscess: reappraisal.
factors.
Al-
though the PET bone scan is anatomically and quantitatively more precise than the MDP scan, it is not more specific for osteomyelitis. Because neoplasms tend to metabolize glucose to a greater extent than do inflammatory processes, the added
creases
Fig. 15.-Abscess, complicating total hip arthroplasty, shown by 111ln-WBC scan. Fever and thigh pain developed 10 years after surgery in a 62-year-old man. Aspiration of joint yielded Staphylococcus aureus. 111In-WBC scan shows an intense focus of activity (arrow) in abscess.
(FOG)
in-
acteristics
VD, London J, Cone AO III. Ring sequestrum: radiographic charof skeletal fixation pin-tract osteomyelitis. Radiology Radiol-
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3. Yuh WTC, Carson JD, Baraniewski
HM, et al. Osteomyelitis
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film, “Tc-MDP
of the foot in
scintigraphy,
imaging in osteomyelitis.
Semin
and NucI