Molecular imaging in musculoskeletal infections with 99mTc-UBI 29-41 SPECT/CT
Molecular imaging in musculoskeletal infections with 99mTc-UBI 29-41 SPECT/CT
Mike Sathekge 0 1 2
Osvaldo Garcia‑Perez 0 1 2
Diana Paez 0 1 2
Noura El‑Haj 0 1 2
Taylor Kain‑Godoy 0 1 2
Ismaheel Lawal 0 1 2
Enrique Estrada‑Lobato 0 1 2
0 International Atomic Energy Agency , Vienna , Austria
1 Nuclear Medicine Department, National Cancer Institute in México , Mexico City , Mexico
2 Department of Nuclear Medicine, University of Pretoria and Steve Biko Academic Hospital , Private Bag X169, Pretoria 0001 , South Africa
3 Mike Sathekge
Objective To determine the added value of CT over planar and SPECT-only imaging in the diagnosis of musculoskeletal infection using 99mTc-UBI 29-4. Materials and methods 184 patients with suspected musculoskeletal infection who underwent planar and SPECT/CT imaging with 99mTc-UBI 29-41 were included. Planar, SPECT-only and SPECT/CT images were reviewed by two independent analysts for presence of bone or soft tissue infection. Final diagnosis was confirmed with tissue cultures, surgery/histology or clinical follow-up. Results 99mTc-UBI 29-41 was true positive in 105/184 patients and true negative in 65/184 patients. When differentiating between soft tissue and bone infection, planar + SPECT-only imaging had a sensitivity, specificity, positive predictive value, negative predictive value and accuracy of 95.0, 74.3, 84.8, 91.3 and 86.9%, respectively, versus 99.0, 94.5, 92.5, 98.5 and 94.5% for SPECT/CT. SPECT/CT resulted in a change in reviewers' confidence in the final diagnosis in 91/184 patients. Inter-observer agreement was better with SPECT/CT compared with planar + SPECT imaging (kappa 0.87, 95% CI 0.71-0.85 versus kappa 0.81, 95% CI 0.58-0.75). Conclusion Addition of CT to planar and SPECT-only imaging led to an increase in diagnostic performance and an improvement in reviewers' confidence and inter-observer agreement in differentiating bone from soft tissue infection.
99mTc-UBI 29-41; SPECT/CT; Infection; Musculoskeletal
The diagnosis and localization of musculoskeletal infection
remains a challenge for physicians as infectious diseases can
be difficult to detect [
]. Molecular imaging now plays a
critical role in the diagnosis of musculoskeletal infections.
Radiolabelled leukocyte or white blood cell (WBC)
imaging is a common modality for infection diagnosis. Its
excellent diagnostic performance has led to it being considered
as the gold-standard imaging modality for peripheral bone
osteomyelitis. However, the process of using radiolabelled
WBCs has also had a fair number of drawbacks [
include the need to collect and label individual patient’s
blood followed by reinjection, the need for a team of
welltrained staff to perform in vitro labelling as well as sufficient
facilities, the risk of acquiring an infection and/or
cross-contaminating samples, and the cost required for cell labelling.
In response to these challenges, significant steps have been
taken over the past decade in identifying and developing
a suitable replacement for WBCs. Advances with
antimicrobial peptides have shown promising developments, the
most promising being ubiquicidin (UBI), a cationic,
synthetic antimicrobial peptide fragment. Labelled with 99mTc,
99mTc-UBI 29-41 has shown a high labelling yield (> 90%)
and proven stability, along with an increased biological and
pharmacological performance, making it a credible
candidate for infection imaging [
Many studies have reported on the use of planar
imaging alone [
]. Lack of anatomic correlation may hamper
delineation of bone infection from adjacent soft tissue
infection. Single-photon emission computed tomography
(SPECT) has better sensitivity compared to planar images
due to enhanced image contrast. Addition of complementary
CT imaging in the form of SPECT/CT has been shown to
improve diagnostic accuracy and interpreters’ confidence
]. CT provides anatomic correlation for the metabolic
imaging allowing clear delineation between contiguous
structures. The aim of this study was, therefore, to assess the
added value of CT over planar and SPECT-only in
radionuclide imaging of musculoskeletal infection with 99mTc-UBI
Materials and methods
One hundred and eighty-four patients (101 women and 83
men; age range 23–85 years; mean age 52.7 years) with
suspected bone and soft tissue infections were enrolled. All
patients exhibited clinical signs of infection (i.e. swelling,
pain, heat, erythema, fever) and abnormal laboratory test
results (increased white blood cell count, percentage of
neutrophils, erythrocyte sedimentation rate). No patient was on
antibiotic therapy prior to scintigraphy. All patients provided
a written informed consent prior to enrollment. The
demographic and clinical characteristics of the patients are
summarized in Table 1. This retrospective study was approved
by the institution’s ethics committee and has been performed
in accordance with the ethical standards laid down in the
1964 Declaration of Helsinki and all subsequent revisions.
Number of patients/average
36 ± 15 mm/hr
104.8 mg/dL ± 35
9. 0 ± 8.2
Synthesis of 99mTc‑UBI 29‑41
99mTc-UBI 29-41 was prepared according to the
recommendations of the IAEA publication on the reconstitution of cold
kits supplied by the National Institute of Nuclear Research.
These steps are as described by Sepúlveda-Méndez et al.
]. Briefly, Tc-99m sodium pertechnetate (370 MBq in
0.5 ml 0.9% saline) was added to a vial containing 25 mg
UBI (29-41) peptide, 10 µl 0.01 M acetic acid, stannous
ions, and 20 µl sodium borohydrate (8.0 µl, 0.7 mg/ml in
0.1 N NaOH). The solution was allowed to stand at room
temperature for 30 min. Quality control of each synthesis
was done using instant thin-layer chromatography (ITLC).
Whole-body and static images were obtained 30 min after
injection of 555–725 MBq of 99mTc-UBI 29-41. SPECT/
CT images were obtained over the region of interest 60 min
SPECT imaging was performed using a Symbia T6
gamma camera (Siemens Medical Solutions, Hoffman
Estates, Illinois) equipped with low-energy and
ultrahighresolution collimator. The energy peak was centred at
140 keV with a window of 15% and the use of non-circular
orbit. Zoom was 1×, 128 steps 30 s each and a matrix size
of 128 × 128 pixels. Image reconstruction was done with
ordered subset expectation maximization (OSEM) iterative
reconstruction (4 iterations and 8 subsets). The CT study
was performed using a Siemens Sensation 6-detector
(Siemens Medical Solutions, Hoffman Estates, Illinois) with a
kilovoltage of 140 keV and 100 mA/s, speed of 0.6 s,
collimation of 0.75 mm and reconstruction Kernel filter B2f
images using filtered back-projection to produce
cross-sectional images covering the same area of the SPECT study.
Both CT attenuation-corrected and non-corrected SPECT
images were sent in DICOM format (Digital Imaging and
Communication in Medicine) to a Siemens multi-modality
workstation to be reconstructed and fused using the Syngo
MI software (Siemens Medical Solutions, Hoffman Estates,
Illinois). Images were evaluated in the coronal, transaxial,
and sagittal planes and in tridimensional
maximum-intensity-projection cine mode by the application Syngo TrueD
(Siemens Medical Solutions, Hoffman Estates, Illinois)
Image analysis and interpretation
Two experienced nuclear medicine physicians unaware of
the patients’ clinical history and results of prior
conventional imaging independently reviewed the planar scans
and SPECT/CT images with regard to the presence and
location of any focus of abnormal accumulation indicating
infection. Preliminary analysis of the SPECT/CT images
included visual inspection to exclude misregistration
between the SPECT and the CT components.
On the images, anatomically adjusted regions of interest
were drawn over the entire focus of infection (target [T])
and contralateral (non-target [NT]) area. Accumulation of
the tracer at sites of infection was expressed as a ratio of
number of counts in the target and non-target areas (T/
The images were classified as negative when no sites
of abnormal uptake were observed and positive when at
least one focus of abnormal uptake was characterized by a
radioactivity level equal to or above that of the liver. Focal
uptake indicating infection was further classified depending
on presence at single or multiple sites.
Semi-quantification of the added value of SPECT/CT
versus SPECT-only was measured using the method described
by Roach et al. [
]. For each abnormality seen on SPECT
or planar imaging, the confidence of the reviewers for both
location and diagnosis was rated using the following
fivepoint scale: (1 = little confidence, 2 = some confidence,
3 = moderate confidence, 4 = good confidence, 5 = high
Both physicians then reviewed each case concurrently and
a consensus was reached in the event of disagreement. The
SPECT/CT-fused images were reviewed at the workstation
and the same assessment of lesion location and diagnosis
was made. The confidence for both location and diagnosis
was recorded using the same five-point scale as previously
stated. When determining whether there was more
information provided by SPECT/CT versus SPECT-only, a change
in confidence of at least two points on the five-point scale
was required to imply significance.
When determining whether the SPECT/CT had resulted
in a change in reviewers’ confidence in the final diagnosis
and scan interpretation, a three-point scale was used with
0 indicating no change, 1 indicating a minor change, and 2
indicating a major change.
Data analysis and statistics
The results of 99mTc-UBI 29-41 scintigraphy were verified
for each suspected site with tissue cultures (121 patients),
surgery plus histology (17 patients) or by clinical follow-up
of up to 6 months (46 patients) with an additional clinical
follow-up of up to 12 months.
Initially, SPECT and planar images were separately
assessed by the two nuclear medicine physicians unaware
of the results of any prior tissue culture and radiologic
investigations (CT or MRI). Hybrid imaging was subsequently
evaluated, and the SPECT/CT findings were compared
against findings obtained with planar and SPECT-only
imaging. SPECT/CT was considered contributory if it accurately
localized the anatomic site of infection and, in particular, if
it discriminated between bone and soft tissue involvement.
The inter-observer agreement levels were assessed with a
All values were expressed as median and range, as
customary for nonparametric data. Sensitivity and specificity
of 99mTc-UBI 29-41 planar, SPECT-only, and SPECT/CT
imaging were calculated based on the final diagnosis.
The radiochemical purity was greater than 95% in all
syntheses. No additional purification was necessary after kit
preparation. No adverse reaction was observed following
99mTc-UBI 29-41 administration to patients.
99mTc-UBI 29-41 scintigraphy was true positive for
infection in 105 out of 184 patients and true negative in
65 out of 184 subjects. When differentiating between soft
tissue versus bone infection, combined planar and SPECT
imaging had a sensitivity of 95.0%, a specificity of 74.3%,
a positive predictive value of 84.6%, a negative
predictive value of 91.3%, and an accuracy of 86.9% (Figs. 2a,
3a). SPECT/CT, on the other hand, had a sensitivity of
99.0%, a specificity of 94.5%, a positive predictive value
of 92.5%, a negative predictive value of 98.5%, and an
accuracy of 94.5% (Figs. 2b, c; 3B).
Target to non-target area ratios (T/NT) were
calculated at 60 min post-injection, analysed by ROC curves
with a cut-off measure of 2.55± 0.7, a sensitivity of 100%
(95% CI 63–100%), and a specificity of 97.8% (95% CI
82.47–99.94%) to differentiate between infection and
non-infected areas. Furthermore, the inter-observer
agreement level was higher for SPECT/CT (kappa 0.87, 95%
CI 0.71–0.85) than for SPECT-only (kappa 0.81, 95% CI
SPECT/CT contribution to final diagnosis
The interpretation of conventional scintigraphy
(planar + SPECT) was changed on the basis of SPECT/CT in
91 of the 184 patients (49.4%). This change in interpretation
was minor in 11.4% of patients and major in 38% of patients
(Table 2). Osteomyelitis was excluded in 36 patients and
the extent of infection was more accurately assessed in 27
Of the microorganisms identified, Staphylococcal species
were most frequently responsible for infections (n = 47/109),
followed by Pseudomonas aeruginosa (n = 18/109),
Escherichia coli (n = 18/109), and (n = 16/109) for Enterococcus
fecalis. There were 13 patients with polymicrobial infection.
In this study, we report on the added value of complementary
CT imaging to planar and SPECT-only imaging of
musculoskeletal infection using 99mTc-UBI 29-41. To our knowledge,
this is one of the largest studies that have described this
imaging modality in musculoskeletal infection and the first
to have reported on the added value of complementary
morphologic imaging with CT. UBI 29-41, as a cationic human
antimicrobial peptide, has a high sensitivity and specificity
for the detection of bacterial and fungal infections in both
human and animals, including immunocompromised
]. The Coordinated Research Project (CRP)
established by the IAEA over the past decade has encouraged the
evaluation of UBI as an effective tracer. Studies under the
CRP and others have reported UBI to exhibit a high labelling
efficiency >90%, good stability, rapid uptake and clearance
via the kidneys, excellent ability to detect infection focus
and its differentiation from sterile inflammation as well as
therapy response assessment [
Detection of osteomyelitis on 99mTc-UBI 29-41 planar
scans alone without anatomic landmarks may be difficult.
The accuracy of imaging may be compromised when
attempting to differentiate between bone and soft tissue
infection as 99mTc-UBI 29-41 accumulates in soft tissue
infection as well (Fig. 1a) [
We clearly demonstrate better accuracy with SPECT/
CT imaging compared to planar and SPECT-only
imaging, 94.5 versus 86.9%. The better accuracy of SPECT/CT
imaging lies in its higher specificity compared to planar
and SPECT-only imaging, 94.5 versus 74.3%. Both
imaging techniques show satisfactory sensitivity of 95.0% for
planar and SPECT-only imaging and 99.0% for SPECT/
CT imaging. Sepúlveda-Méndez et al. evaluated the role
of 99mTc-UBI 29-41 scintigraphy in identifying focus
of infection in patients with fever of unknown origin
]. They reported a sensitivity of 97.52%, a specificity
of 95.35%, and an accuracy of 96.62%. Another study
explored the use of 99mTc-UBI 29-41 scintigraphy in
diabetic foot infections and reported perfect sensitivity,
specificity and accuracy values of 100% [
]. Inclusion of bone
scan for anatomic correlation to differentiate bone
infection from infection limited to the soft tissue in the latter
study is probably responsible for this excellent diagnostic
A more recent study which also used 99mTc-MDP bone
scan to correlate findings on 99mTc-UBI planar imaging
reported sensitivity, specificity, PPV and NPV of 100, 85.7,
93.75, 100%, respectively, in 22 patients with painful
prostheses evaluated for septic loosening [
]. The perfect NPV
reported in this study may be attributed to the inclusion of
bone scan in image interpretation. While bone scan has poor
specificity for the detection of infection in a violated bone, it
has an excellent negative predictive value. The inclusion of
99mTc-MDP bone scan in some of these studies emphasizes
the need for some anatomic correlation.
The independent reviews conducted by two nuclear
medicine physicians reported a significant increase in confidence
in regard to final diagnosis and localization of infection.
After an initial evaluation of the planar and SPECT-only
imaging, subsequent review of the SPECT/CT imaging
resulted in a change in reviewers’ confidence in diagnosing
the presence of infection and differentiating between bone
and soft tissue infection in 49.4% of patients. The change in
confidence was major in 38% of patients. Complementary
anatomic CT imaging is important in delineating
osteomyelitis from infection in adjacent soft tissue. This
differentiation has management implication as both types of infection
may be treated differently. Roach et al. evaluated the impact
of inclusion of CT for anatomic correlation in a diverse type
of radionuclide imaging and reported an overall change in
reviewers’ confidence with regard to lesion localization and
in the final diagnosis in 56% of patients on the basis of
inclusion of CT information [
Addition of CT data in image interpretation led to
improvement in inter-observer agreement in differentiating
soft tissue from bone infection; SPECT/CT kappa 0.87,
95% CI 0.71–0.85 and planar, and SPECT-only imaging
kappa 0.81, 95% CI 0.58–0.75.
Positron emission tomographic (PET) imaging has
better resolution than the SPECT system. The PET systems
are now mostly hybrid in the form of PET/CT and more
recently PET/MR. The better resolution of the PET camera
and complementary anatomic information available from
CT has led to interest in 68Ga-labelled UBI 29-41 for PET
imaging of infection [
]. The added value of SPECT/
CT and PET/CT for diagnosing infections may ultimately
increase the usefulness and accuracy of the highly specific
UBI tracer by increasing its ability to provide precise
anatomical locations as well as improve spatial resolution.
In an effort to improve target/non-target ratios (T/NT),
a critical step during the molecular imaging process is
determining at what time scans should be taken. There is a
great diversity in the imaging time as reported in different
]. In our study, we obtained the planar images
at 30 min and the SPECT/CT images 60 min post-tracer
injection. In ROC analysis, we obtained a T/NT cut-off
ratio of 2.55 ± 0.7 at 60 min post-tracer injection with a
sensitivity of 100% (95% CI 63–100%), and a specificity
of 97.8% (95% CI 82.47–99.94%) to differentiate between
infected and non-infected areas. Melendez-Alafort et al.
observed a T/NT ratio of 2.18 ± 0.74 in positive lesions
after 120 min and minimal accumulation in non-target
]. In a group of 50 patients with suspected
musculoskeletal infection, Esmailiejah and colleagues reported
a T/NT ration (lesion to background ratio) of 2.05 ± 0.41
in infection site which was significantly higher than T/
NT ratio found at sites negative for infection (1.52 ± 0.22,
p < 0.001) [
]. In their study, whole-body planar images
were acquired at 60 and 120 min post-tracer injection. It
is unknown on which of the two images acquired at 60 and
120 min the T/NT ratio was calculated from. This makes
comparison of their T/NT ratios with those of other
studies difficult. Our T/NT cut-off ratio obtained at 60 min
post-tracer injection appears to have sufficient sensitivity
and specificity to differentiate between infection and its
absence. We, therefore, speculate that a waiting period
of 60 min prior to imaging is sufficient and that it may be
unnecessary to wait for 120 min post-tracer injection for
In conclusion, 99mTc-UBI 29-41 scintigraphy has an
excellent diagnostic performance in the evaluation of
musculoskeletal infection. Addition of CT morphologic
imaging to planar and SPECT-only imaging led to an
increased in diagnostic performance and an improvement
in diagnostic confidence in differentiating soft tissue
from bone infection as well as a higher inter-observer
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