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1 Department of Medical Radiology, Nuclear Medicine, University Hospital,
Ramistr. 100, CH-8091 Zurich, Switzerland.
2 Department of Radiology, Orthopedic University Hospital Balgrist, Forchstr.
340, CH-8008 Zurich, Switzerland.
3 Department of Diagnostic Radiology, University Hospital, Zurich,
Switzerland.
4 Department of Orthopedic Surgery, Orthopedic University Hospital Balgrist,
Zurich, Switzerland.
Received November 12, 2001;
accepted after revision May 7, 2002.
Address correspondence to G. K. von Schulthess.
Abstract
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SUBJECTS AND METHODS. FDG PET was performed prospectively in 30
consecutive patients with substantial endplate abnormalities (craniocaudal
diameter of bone marrow abnormalities, 
25% of vertebral height) found
during MR imaging of the lumbar spine. Both the MR and PET images were
evaluated by two experienced musculoskeletal radiologists and two experienced
nuclear physicians. The diagnosis of either degeneration with different types
of endplate abnormalities or disk-space infection was determined. Clinical
follow-up and, in selected cases, bone biopsies with cultures were used as the
standard of reference.
RESULTS. On the MR images, 25 of the 38 degenerated levels were classified as Modic type I, 13 levels as type II, and none as type III. Five disk-space infections were diagnosed in four patients. MR imaging findings were false-positive at one disk level with type I abnormalities and false-negative at two levels with infection. PET did not show FDG uptake in the intervertebral spaces of any patient with degenerative disease. FDG PET findings were true-positive in all five levels with disk-space infection. The sensitivity and specificity for MR imaging in detecting disk-space infection were 50% and 96%, and were 100% and 100% for FDG PET, respectively (not significant, McNemar test, p = 0.5).
CONCLUSION. Our findings suggest that FDG PET may prove useful for differentiation of degenerative and infectious endplate abnormalities detected on MR imaging. Even in active (Modic type I) degenerative endplate abnormalities in our series, PET did not show increased FDG uptake.
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Positron emission tomography (PET) with FDG has increasingly been used in suspected infection. The pathophysiologic basis of FDG PET in determining infectious disease may relate to a so-called respiratory burst that neutrophilic and eosinophilic granulocytes, as well as mononuclear phagocytes, experience when exposed to proinflammatory cytokines (e.g., granulocyte—macrophage colony stimulating factor, interleukin-8, and interleukin-6), with the resulting metabolization of large amounts of glucose [6]. FDG PET appears to be sensitive in the diagnosis of infection of the musculoskeletal system. Because data about true-negative results are difficult to obtain, specificity has not been equally well documented [7,8,9]. FDG PET should be able to differentiate degenerative from infectious endplate abnormalities because granulocytes and macrophages with their respiratory bursts are not a prominent feature in degeneration [10, 11]; thus, less FDG uptake would be expected.
The purpose of this investigation was to evaluate the usefulness of FDG PET for differentiation of degenerative and infectious endplate abnormalities.
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25% of vertebral height). Patients with signal abnormalities limited to
having previous surgery, recent fracture, metastatic disease, spondylolysis,
and pregnancy were excluded. From the 37 eligible patients, seven were excluded for the following reasons: Two patients (29 and 32 years old) were not willing to undergo a PET examination because of the associated radiation exposure. Two patients refused further investigation because of a lack of time. Another three patients did not arrive for the PET appointment.
The remaining 30 patients underwent FDG PET examinations within 7 days of MR imaging. Eleven of the 30 patients were men, and 19 were women. Their mean age was 54 years (range, 27-80 years). In the 30 patients, a total of 43 levels with substantial MR imaging abnormalities were evaluated. Seven patients had symptoms persisting for less than 6 weeks, and 23 patients, for more than 6 weeks. In seven of the 30 patients, an infection was originally suspected by the referring clinician.
A total of five patients underwent surgery. In three patients, lower spine osteosynthesis was performed, and in two, surgical biopsy. The study was approved by the institutional review board, and written informed consent was obtained from all patients.
MR Imaging Protocol
MR imaging was performed on a 1.0-T scanner (Expert; Siemens Medical
Solutions, Erlangen, Germany) with a dedicated phased array spine coil.
Sagittal T1-weighted (TR/TE, 700/12) and sagittal T2-weighted fast spin-echo
(5000/112) sequences were obtained with an image matrix of 512 x 210 or
512 x 192, a field of view of 300 x 225 mm or 300 x 180 mm,
and a section thickness of 4 mm. In addition, axial T2-weighted fast spin-echo
sequences (4000/96) were obtained with an image matrix of 512 x 192, a
field of view of 150 mm, and a slice thickness of 4 mm. When the radiologist
responsible for the MR imaging examination suspected disk-space infection on
the basis of either the clinical findings, the findings from the standard MR
images, or both, and considered IV contrast agents to be potentially
contributing to the diagnosis, the radiologist obtained either sagittal or
coronal fat-suppressed T1-weighted images after the IV injection of
gadopentetate (0.1 mmol/kg of body weight) (n = 17). A total of 14
patients had such injections. In two patients referred from an outside
institution, MR imaging was performed on a 1.5-T scanner (General Electric
Medical Systems, Milwaukee, WI) with similar parameters.
Evaluation of MR Images
All MR images were evaluated in conference by two experienced radiologists
specializing in MR imaging of the musculoskeletal system. The observers were
unaware of clinical and other imaging findings. In one case, observer
disagreement occurred that was resolved by a third experienced
radiologist.
The abnormal levels were classified as either infected or degenerative (Modic type I, II, or III abnormalities) [2]. Modic type I changes are characterized by hypointensity on T1-weighted and hyperintensity on T2-weighted images; type II changes, by hyperintensity on T1-weighted and iso- or hyperintensity on T2-weighted images; and type III changes, by hypointensity on both T1- and T2-weighted images. The disk had to be hypointense on T2-weighted images, although a thin hyperintense line in the central disk (presumably corresponding to fluid entering a degenerative central disk gap) was also accepted as degenerative. If contrast material had been applied, no enhancement should have been present either in the disk or in the adjacent soft tissue. If two types of degenerative endplate abnormalities were found in an intervertebral space, the larger of the two abnormalities determined the diagnosis. When their size was identical, type I abnormalities had first priority; type II abnormalities, second priority; and type III abnormalities, third priority [12].
Disk-space infection was diagnosed in the presence of paravertebral or epidural signal abnormalities with or without abscess formation [13]. If such findings were absent, three of the following four criteria had to be fulfilled for disk-space infection: signal abnormality of the bone marrow adjacent to the intervertebral disk (hypointense on T1-weighted images and hyperintense on T2-weighted images, signal not well demarcated); loss of the low-intensity vertebral endplate on T1-weighted images [14]; hyperintensity of the disk on T2-weighted images [13]; and disk enhancement after injection of gadopentetate.
PET Protocol
FDG PET studies were performed on an Advance PET scanner (General Electric
Medical Systems, Waukesha, WI) using the whole-body mode. Several data sets
with 35 two-dimensional sections of 4.25-mm thickness with an axial field of
view of 14.6 cm each were acquired, covering the body from the head to the
pelvic floor. The patients fasted for at least 4 hr before the study. Thirty
to forty minutes before scanning, the patients received an IV injection of
300-400 MBq of FDG that was produced in-house using a 17.8-MeV cyclotron (PET
Trace 2000; General Electric Medical Systems, Uppsala, Sweden) and an
automated FDG synthesis module (Nuclear Interface PET Tracer Synthesizer;
Muenster, Germany). Corrected and uncorrected axial images were acquired. A
multiplicative iterative reconstruction algorithm was used for improvement of
image quality and reduction of computation time
[15]. We also obtained coronal
and sagittal reformations.
Evaluation of PET Images
Image analysis was performed on a digital viewing system (Extended Viewing
Station; General Electric Medical Systems). The PET scans were analyzed by two
experienced nuclear physicians in conference who were unaware of clinical and
other imaging findings. They were aware, however, that lumbar endplate changes
had been found on at least one level during MR imaging. Disk-space infection
was differentiated from degeneration if increased FDG accumulation was present
in either the vertebral disk or the adjacent vertebral body (qualitative
evaluation).
Standard of Reference
Disk-space infection was considered to be present when cultures from the
bone biopsies (n = 2) or blood were positive (n = 1). In two
cases, disk-space infection was diagnosed on the basis of clinical and
laboratory findings (elevated erythrocyte sedimentation rate and C-reactive
protein) and imaging follow-up. Disk-space degeneration was considered to be
present when the findings from the laboratory data and the clinical signs
(n = 23) were negative after 6 months or when surgical findings
(n = 3) were negative.
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In the five intervertebral disk spaces with infection, MR imaging findings were false-negative at two levels and true-positive at three levels. In one patient, two disk levels were infected, one of which was correctly diagnosed as infection, the other as degeneration. Therefore, on a per patient basis we had two false-negative, one false-positive, and two true-positive cases, and the sensitivity and specificity for MR imaging in detecting disk-space infection were 50% and 96%, respectively. Both false-negative levels had equivocal, centrally located disk hyperintensity on T2-weighted images but no disk or soft-tissue contrast enhancement (Fig. 2A,2B,2C,2D). Neither clinical nor laboratory findings of infection were present. The diagnosis of disk-space infection in the two false-negative cases were made by bone and blood culture findings of coagulase-positive Staphylococcus organisms in one patient and Escherichia coli in the blood culture in the other patient.
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The potential diagnostic dilemma in the differentiation of degenerative endplate abnormalities from early disk-space infection is shown in Figures 1A,1B,1C,1D and 2A,2B,2C,2D, which reveal endplate abnormalities and disk hyperintensity on T2-weighted images.
MR imaging findings were positive in two of the seven patients with clinical suspicion of infection.
PET
FDG accumulation was found in all five levels with disk-space infection
(Figs.
2A,2B,2C,2D
and
3A,3B,3C,3D).
Therefore, FDG PET findings were true-positive at all five disk levels. FDG
accumulation was absent at all disk levels with degenerative disease diagnosed
on MR images, including both Modic type I and Modic type II endplate
abnormalities. Therefore, FDG PET findings were true-negative in all patients
with degenerative disk disease. No false-positive or false-negative diagnosis
was made with PET (Fig.
1A,1B,1C,1D).
Both the sensitivity and specificity for FDG PET in detecting disk-space
infection were 100%. The statistical power of this result is not sufficient to
reach a definitive conclusion, however (McNemar test, p = 0.5).
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In all patients with positive findings on FDG PET images, the referring clinician had originally suspected infection.
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The following criteria used for differentiation of degeneration from infection on MR images are not consistently present: the disk form is more commonly altered and shows more peripherally located and more extensive enhancement in infection than in degeneration [18]; and, in infection, disk signal on T2-weighted images or short tau inversion recovery images is more commonly increased when compared with patients who have degeneration (prevalence of hypointense disk signal in degeneration, 82.1%) [14].
Our false-positive MR imaging diagnosis was made in a disk with both increased signal intensity on T2-weighted images and substantial enhancement after IV injection of contrast material (Fig. 1A,1B,1C,1D). One of the two false-negative diagnoses was made in the presence of a type I abnormality, the other in the presence of both type I and type II abnormalities (Fig. 2A,2B,2C,2D).
FDG PET is sensitive in diagnosing infection [7,8,9, 19,20,21,22,23,24]. Our results showing positive findings on PET scans in all patients with disk-space infection confirm these results. A few reports [25,26,27] indicate that noninfectious inflammatory disease may also be associated with radiotracer uptake that would reduce specificity. Because none of our patients with a degenerated disk space showed FDG uptake, even in the presence of substantial Modic type I abnormalities, FDG PET may be useful for excluding disk-space infection in cases of equivocal MR imaging findings. FDG PET scans also appears to be superior to bone scans that are nonspecific in this situation [3].
The specificity of FDG PET may be explained on the basis of histology and pathophysiology. Granulocytes and macrophages are commonly present in infection but not in degeneration. These cell types are characterized by respiratory bursts when activated by inflammatory mediators present in infectious foci, which results in increased glucose metabolism [6, 19, 28]. The matured fibroblasts that are a typical constituent of granulation tissue [29, 30] and therefore potentially found in degeneration do not react with such respiratory bursts. Daley et al. [31] found that the cells present after sterile injury were predominantly fibroblasts. Macrophages accounted for fewer than 10% of cell types in this investigation.
Our study has limitations. For obvious reasons, a bone biopsy sample is not normally obtained in patients with degeneration, and clinical follow-up had to be used as a standard of reference. In addition, the prevalence of disk-space infections is low, which relates to the prospective nature of this study. Calculated sensitivity and specificity values should not be overinterpreted. However, the fact that no positive findings on PET scans were revealed in a relatively large number of degenerative endplate abnormalities with substantial extension indicates that FDG PET is probably specific in excluding the diagnosis of disk-space infection. The high specificity of FDG PET in the diagnosis of disk-space infection cannot easily be reconciled with the previously mentioned concept of inflammatory degeneration proposed by Burke et al. [17], which may result in overlapping histologic features. Lower specificities may be reported in the future when larger series of patients become available. Moreover, the difficult problem of distinguishing surgically induced endplate abnormalities from infection has not been addressed with our study design.
In conclusion, our findings suggest that FDG PET may prove useful for differentiation of degenerative and infectious endplate abnormalities found on MR imaging. Even in active (Modic type I) degenerative endplate abnormalities in our series, PET did not show increased FDG uptake.
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