Characterization of Focal Bone Lesions in the Axial Skeleton: Performance of Planar Bone Scintigraphy Compared with SPECT and SPECT Fused with CT
Abstract
OBJECTIVE. The purpose of this study was to evaluate the diagnostic performance of planar 99mTc methylene diphosphonate bone scintigraphy compared with SPECT and SPECT fused with CT in patients with focal bone lesions of the axial skeleton.
SUBJECTS AND METHODS. Thirty-seven patients with 42 focal lesions of the axial skeleton were included in this prospective study. All patients underwent planar scintigraphy, SPECT through the focal lesions, and SPECT-guided CT. SPECT and CT images then were fused digitally. The three types of images were evaluated separately from one another by two experienced reviewers working to consensus. Visibility of the lesions, diagnostic performance, and certainty in diagnosis were evaluated. Performance for specific diagnoses also was evaluated. Histologic, MRI, and clinical follow-up findings were used as the reference standard.
RESULTS. Visibility of the lesions was significantly better with SPECT than with planar scintigraphy (p < 0.0001). Sensitivity and specificity for differentiation of benign and malignant bone lesions were 82% and 94% for planar scintigraphy, 91% and 94% for SPECT, and 100% and 100% for SPECT fused with CT. Differences between the three methods of differentiating benign and malignant lesions did not reach statistical significance. Certainty in diagnosis was significantly higher for SPECT fused with CT than for planar scintigraphy (p = 0.004) and SPECT (p = 0.004). A specific diagnosis was made with planar scintigraphy in 64% of cases, with SPECT in 86%, and with SPECT fused with CT in all cases.
CONCLUSION. Planar scintigraphy may suffice for differentiating benign and malignant lesions of the axial skeleton, but SPECT fused with CT significantly increases certainty in diagnosis and is the best tool for making a specific diagnosis.
Introduction
Bone scintigraphy is still the work-horse of nuclear medicine in the search for bone metastasis in patients with malignant tumors, especially prostate and breast cancer. Bone scintigraphy is widely available, relatively inexpensive, and highly sensitive in the detection of bone metastasis. The high sensitivity correlates with a lower specificity because many benign conditions, such as degenerative joint disease, infections, and benign bone tumors, exhibit increased uptake of radiotracer [1].
The combination of functional and morphologic findings with PET/CT increases the diagnostic performance of PET alone [2-4]. Similarly, SPECT/CT promises to overcome the insufficient specificity of planar scintigraphy and SPECT alone [5-7]. SPECT improves lesion to background contrast enhancement and allows detailed anatomic localization. SPECT thus promises to be useful in imaging of complex anatomic regions such as the spine. Fused SPECT/CT images can be obtained with integrated SPECT/CT scanners, in which CT data are used for attenuation correction, and with software fusion of SPECT and CT data obtained with two separate scanners [5, 6]. MDCT rapidly provides detailed morphologic information about osseous structures. The aim of this study was to evaluate the diagnostic performance of planar 99mTc methylene diphosphonate bone scintigraphy compared with SPECT and fused SPECT and 64-MDCT data obtained with separate systems in patients with focal lesions of the axial skeleton.
Subjects and Methods
Patients
Between August 2005 and December 2005, a total of 37 consecutively enrolled patients (20 women, 17 men; mean age, 64.4 years; age range, 34-83 years) with foci of abnormal radiotracer uptake in the axial skeleton on planar bone scintigraphy were included in this prospective study. Written informed consent in accordance with the regulations of the institutional review board had been given by all patients before CT data acquisition. Forty-two focal lesions of the axial skeleton in the following locations were evaluated: spine (n = 30), sternum (n =1), rib (n = 2), sacrum (n = 7), acetabulum (n = 1), and mandible (n =1). Thirty patients had underlying malignant disease (Fig. 1A, 1B, 1C, 1D, 1E, 1F, 1G, 1H) (16, breast cancer; nine, prostate cancer; two, otolaryngologic cancer; one, esophageal cancer; one, lymphoma; one, renal cell cancer), and seven patients had skeletal pain (Figs. 2A, 2B, 2C, 2D, 2E, 2F, 2G, 2H and 3A, 3B, 3C, 3D, 3E).
Planar Bone Scintigraphy
All patients underwent whole-body bone planar scintigraphy in the anterior and posterior positions 3 hours after injection of 450 MBq of 99mTc methylene diphosphate. Scintigraphy was performed with a dual-head system (Millenium VG, GE Healthcare) equipped with a low-energy high-resolution parallel-hole collimator.
SPECT
After completion of planar scintigraphy, all patients underwent SPECT with the gamma camera used for scintigraphy. The detectors were positioned on the focal lesions localized with planar scintigraphy. SPECT data were collected in step-and-shoot mode with an angular range of 180° in 3° increments and a duration of 30 seconds each. Projection data were collected with a zoom factor of 1 and a 128 × 128 matrix size. SPECT images were iteratively reconstructed with an ordered subset expectation maximization algorithm implemented on a clinical workstation (Xeleris 1.221, GE Healthcare). The final pixel size was 4.42 mm in all directions.
CT
After SPECT data collection, patients were transferred to a standalone 64-MDCT scanner (Lightspeed VCT, GE Healthcare). Care was taken to reproduce exactly the same patient position as for the SPECT acquisition. Unenhanced CT was performed in helical mode with a table speed of 10.6 mm/rotation and a rotation time of 0.6 second. The other scan parameters depended slightly on the clinical situation. A voltage of 120 or 140 kV was used, and the current was automatically adjusted in the range of 100-700 mA, depending on the setting of a noise index ranging from 24 to 33. No IV contrast material was injected. CT images were reconstructed with the standard parameters and reviewed in the bone window. To improve contrast enhancement, CT images were reformatted as maximum intensity projection images in the sagittal and coronal planes with an in-plane pixel size of 0.7 mm and a slice thickness of 5 mm.
SPECT and CT Image Fusion
All images were transferred to a workstation running software for quantitative analysis (PMOD v2.65, PMOD Technologies). We interactively matched the SPECT images to the CT maximum intensity projection images by bringing internal anatomic landmarks (e.g., iliac crest) into agreement. To confirm the matching quality, we inspected fusion images in all directions (transverse, coronal, sagittal).
Image Interpretation
Planar scintigraphy, SPECT, and fused SPECT and CT images were evaluated by two experienced reviewers in consensus. One reviewer was double board certified in nuclear medicine and radiology, and the other was board certified in radiology with special training in musculoskeletal radiology and had 3 years of experience in nuclear medicine. The reviewers were blinded to clinical information and medical history. The three types of images were evaluated separately: first the planar bone scintigraphic images, then the SPECT images, and last the fused SPECT and CT images. Visibility of the focal lesions was graded on the following five-point scale: 0, not visible; 1, poor visibility; 2, moderate visibility; 3, good visibility; 4, very good visibility. Diagnostic performance in differentiation of benign and malignant focal bone lesions was reported as sensitivity, specificity, accuracy, and negative and positive predictive values. Certainty in diagnosis was graded on the following three-point scale: 0, undecided; 1, probably correct; 2, most likely correct.
Performance in specific diagnosis of a lesion as benign (e.g., fracture, facet joint osteoarthritis, spondylosis deformans) or malignant also was evaluated. For planar scintigraphy and SPECT, the criteria for classifying a focal bone lesion as malignant were that, first, focal radiotracer uptake greater than in the anterior iliac spine located in a anatomic location typical of a metastasis (pedicle, vertebral body) was considered to indicate malignancy. Second, radiotracer uptake equal to or lower than uptake in the anterior iliac spine and uptake that involved both sides of a joint (facet joint, vertebral body endplates) were considered to indicate a lesion was benign. The additional criteria for the CT part of the fused SPECT and CT interpretation were that osteolytic lesions without sclerosis and osteoblastic lesions were considered malignant and that sclerotic lesions with spondylophytes and disk space narrowing or in the subchondral region of a joint together with joint space narrowing, subchondral cysts, and osteophytes were considered benign. Histologic (one patient), MRI (10 patients), scintigraphic (four patients), CT (five patients), and clinical follow-up findings for at least 12 months (all patients), including tumor markers such as prostate-specific antigen in prostate cancer patients and CA 15-3 in breast cancer patients, were used as the reference standard.
Statistical Analysis
Grades of visibility and certainty were recorded as percentages and mean ± SD. Sensitivity, specificity, accuracy, negative predictive value, and positive predictive value for the diagnosis of malignant or benign focal bone lesion were calculated for planar scintigraphy, SPECT, and fused SPECT and CT. Sign tests were used to analyze differences in diagnostic performance of the three imaging techniques. With Bonferroni correction, p < 0.016 was considered to indicate a significant difference. SPSS 11 software (SPSS) was used for statistical analysis.
Results
Of 42 lesions, 11 were metastatic, 27 degenerative, two posttraumatic, and two benign tumors (Table 1). Visibility of the lesions was significantly better with SPECT than with planar scintigraphy (mean value, 3.6 ± 0.6 vs 2.7 ± 0.6; p < 0.0001). The sensitivity and specificity for differentiation of benign and malignant bone lesions were 82% and 94% for planar scintigraphy, 91% and 94% for SPECT, and 100% and 100% for SPECT fused with CT. Differences between the three methods for differentiation of benign and malignant lesions did not reach statistical significance (Table 2).
| Patient No. | Lesion No. | Patient Age (y) | Lesion Location | Planar Scintigraphy | SPECT | SPECT Fused with CT | Final Diagnosis | Specific Diagnosis |
|---|---|---|---|---|---|---|---|---|
| 1 | 1 | 77 | Mandible | Malignant | Malignant | Malignant | Malignant | Metastasis from prostate cancer |
| 2 | Thoracic spine | Malignant | Malignant | Malignant | Malignant | Metastasis from prostate cancer | ||
| 3 | Rib | Malignant | Malignant | Malignant | Malignant | Metastasis from prostate cancer | ||
| 2 | 4 | 57 | Lumbar spine | Malignant | Malignant | Malignant | Malignant | Metastasis from breast cancer |
| 3 | 5 | 75 | Lumbar spine | Benign | Benign | Benign | Benign | Spondylosis and facet joint osteoarthritis |
| 4 | 6 | 52 | Cervical spine | Benign | Benign | Benign | Benign | Facet joint osteoarthritis |
| 5 | 7 | 69 | Lumbar spine | Benign | Benign | Benign | Benign | Spondylosis |
| 6 | 8 | 57 | Cervical spine | Benign | Benign | Benign | Benign | Facet joint osteoarthritis |
| 9 | Sacrum | Malignant | Malignant | Malignant | Malignant | Metastasis from esophageal cancer | ||
| 7 | 10 | 63 | Lumbar spine | Benign | Benign | Benign | Benign | Spondylosis |
| 8 | 11 | 74 | Lumbar spine | Benign | Benign | Benign | Benign | Osteochondrosis |
| 9 | 12 | 83 | Lumbar spine | Benign | Benign | Benign | Benign | Spondylosis and facet joint osteoarthritis |
| 10 | 13 | 53 | Lumbar spine | Benign | Benign | Benign | Benign | Facet joint osteoarthritis |
| 11 | 14 | 67 | Lumbar spine | Benign | Benign | Benign | Benign | Facet joint osteoarthritis |
| 12 | 15 | 66 | Lumbar spine | Benign | Benign | Benign | Benign | Facet joint osteoarthritis |
| 13 | 16 | 52 | Lumbar spine | Benign | Benign | Benign | Benign | Osteochondrosis |
| 14 | 17 | 67 | Lumbar spine | Benign | Benign | Benign | Benign | Facet joint osteoarthritis |
| 15 | 18 | 52 | Sacrum | Benign | Benign | Benign | Benign | Iliosacral joint osteoarthritis |
| 16 | 19 | 56 | Sternum | Benign | Benign | Malignant | Malignant | Metastasis from breast cancer |
| 17 | 20 | 66 | Lumbar spine | Benign | Benign | Benign | Benign | Spondylosis |
| 18 | 21 | 63 | Sacrum | Benign | Benign | Benign | Benign | Iliosacral joint osteoarthritis |
| 19 | 22 | 72 | Thoracic spine | Malignant | Malignant | Malignant | Malignant | Metastasis from breast cancer |
| 20 | 23 | 78 | Lumbar spine | Benign | Benign | Benign | Benign | Facet joint osteoarthritis |
| 24 | Sacrum | Malignant | Malignant | Benign | Benign | Iliosacral joint osteoarthritis | ||
| 25 | Acetabulum | Benign | Malignant | Malignant | Malignant | Metastasis from prostate cancer | ||
| 21 | 26 | 77 | Thoracic spine | Benign | Benign | Benign | Benign | Spondylosis |
| 22 | 27 | 71 | Sacrum | Benign | Benign | Benign | Benign | Old fracture |
| 23 | 28 | 78 | Thoracic spine | Malignant | Malignant | Benign | Benign | Hemangioma |
| 24 | 29 | 55 | Thoracic spine | Benign | Benign | Benign | Benign | Spondylosis |
| 25 | 30 | 75 | Sacrum | Benign | Benign | Benign | Benign | Iliosacral joint osteoarthritis |
| 26 | 31 | 75 | Lumbar spine | Benign | Benign | Benign | Benign | Spondylosis |
| 27 | 32 | 48 | Thoracic spine | Malignant | Malignant | Malignant | Malignant | Metastasis from breast cancer |
| 28 | 33 | 45 | Sacrum | Benign | Benign | Benign | Benign | Iliosacral joint osteoarthritis |
| 29 | 34 | 55 | Rib | Benign | Benign | Benign | Benign | Old fracture |
| 30 | 35 | 76 | Lumbar spine | Malignant | Malignant | Malignant | Malignant | Metastasis from prostate cancer |
| 31 | 36 | 66 | Thoracic spine | Benign | Benign | Benign | Benign | Giant Schmorl node |
| 32 | 37 | 49 | Thoracic spine | Benign | Benign | Benign | Benign | Spondylosis |
| 33 | 38 | 77 | Lumbar spine | Benign | Benign | Benign | Benign | Spondylosis |
| 34 | 39 | 76 | Lumbar spine | Malignant | Malignant | Malignant | Malignant | Metastasis from breast cancer |
| 35 | 40 | 68 | Lumbar spine | Benign | Benign | Benign | Benign | Spondylosis |
| 36 | 41 | 34 | Lumbar spine | Benign | Benign | Benign | Benign | Melorheostosis |
| 37 | 42 | 59 | Lumbar spine | Benign | Benign | Benign | Benign | Spondylosis |
| Diagnostic Value | Planar Scintigraphy | SPECT | SPECT Fused with CT |
|---|---|---|---|
| Sensitivity | 82 (9/11) | 91 (10/11) | 100 (11/11) |
| Specificity | 94 (29/31) | 94 (29/31) | 100 (31/31) |
| Accuracy | 91 (38/42) | 93 (39/42) | 100 (42/42) |
| Positive predictive value | 82 (9/11) | 83 (10/12) | 100 (11/11) |
| Negative predictive value | 94 (29/31) | 97 (29/30) | 100 (31/31) |
Note—Values are percentages with raw numbers in parentheses.
Certainty in diagnosis of a lesion as benign or malignant was significantly higher with SPECT fused with CT (mean value, 1.9 ± 0.3) than with planar scintigraphy (mean value, 1.0 ± 0.6; p = 0.004) and SPECT (mean value, 1.2 ± 0.6; p = 0.004), but SPECT was not superior to planar scintigraphy (p = 0.25) (Table 3). A specific diagnosis was made with an accuracy of 64% (27/42) with planar scintigraphy, 86% (36/42) with SPECT, and 100% (42/42) with SPECT fused with CT. SPECT fused with CT and SPECT were significantly superior to planar scintigraphy (p = 0.008 and p = 0.0001), but SPECT fused with CT was not significantly superior to SPECT (p = 0.031) for specific diagnosis.
| Technique | Certainty Score (Mean ± SD) | Undecided | Probably Correct | Most Likely Correct |
|---|---|---|---|---|
| Planar scintigraphy | 1.0 ± 0.6 | 9 (21) | 25 (60) | 8 (19) |
| SPECT | 1.2 ± 0.6 | 3 (7) | 27 (64) | 12 (29) |
| SPECT fused with CT | 1.9 ± 0.3 | 0 | 4 (9) | 28 (91) |
Note—Other than certainty score, values are number of cases with percentages in parentheses. SPECT versus planar scintigraphy, not significant; SPECT fused with CT versus planar scintigraphy, p = 0.004; SPECT fused with CT versus SPECT, p = 0.004.
Discussion
Focal lesions in the axial skeleton are significantly better displayed with SPECT and with SPECT fused with CT than with planar bone scintigraphy. Planar scintigraphy may suffice for differentiating benign and malignant lesions. However, SPECT fused with CT significantly increases certainty in diagnosis and is the best tool for making a specific diagnosis [6, 8].
Detection of skeletal metastasis is clinically important because of associated symptoms, complications such as pathologic fractures, and significance for staging, treatment, and prognosis. However, differentiating benign and metastatic bone lesions can be difficult with planar scintigraphy alone. Because of summation of different structures, such as vertebral body, pedicle, and facet and costovertebral joints and because of the high incidence of degenerative changes in the spine, characterization of focal spinal lesions with planar scintigraphy alone can be challenging. SPECT/CT with various radiotracers has been used for indications such as imaging of infection; neuroendocrine tumors; and diseases of the liver, thyroid, and parathyroid glands [5, 9-15]. It has been found that detection and characterization of focal bone lesions improve with SPECT [16-19]. Imaging is moving toward a combination of techniques that yield functional and anatomic information [20, 21]. With the increased availability of integrated SPECT/CT scanners and improved performance of postprocessing image-fusion software, it becomes more and more important to define the indications for fused imaging.
In our study, visibility of the lesions was significantly better with SPECT than with planar scintigraphy. Sedonja et al. [22] performed planar scintigraphy and SPECT on 37 patients with lower back pain without known malignant lesions and on 38 patients with confirmed malignant disease. Overall, significantly more metastatic lesions were detected with SPECT (SPECT, 58 of 64 lesions; planar scintigraphy, 42 of 64 lesions; p < 0.01). These investigators also measured lesion-to-background ratios for malignant lesions of the spine and found a significantly higher ratio with SPECT (2.26) than with planar scans (1.86). Furthermore, our results showed that accuracy in definition of malignant lesions increased from planar scintigraphy to SPECT and to SPECT fused with CT, but the difference in diagnostic performance was not significant. Therefore, planar scintigraphy seems to be sufficiently accurate for determining whether a patient has osseous metastatic disease.
Utsunomiya et al. [6] compared diagnostic confidence in side-by-side interpretation of CT and SPECT data with confidence in interpretation of fused images of patients with suspected bone metastasis and found that interpretation of fused images increases confidence. This finding proves that the process of software fusion is not simply an academic exercise. Similarly, our results showed that the highest degree of confidence in diagnosis is obtained with fused images compared with SPECT alone and with planar scintigraphy alone. With SPECT fused with CT, 91% of diagnoses were made with the highest confidence level (SPECT, 29%; planar scintigraphy, 19%). Confidence in diagnosis is an important factor not only for convincing referring physicians and defending a diagnosis in interdisciplinary meetings but also for avoiding additional expensive imaging such as MRI.
Findings on SPECT fused with CT led to a specific diagnosis in all patients. Often patients with malignant tumors have unclear pain in the skeleton. In these situations, it does not suffice to rule out metastasis. The cause of benign focal uptake should be evaluated carefully because many underlying diseases can influence treatment. Osteoid osteoma can be managed by resection or radiofrequency ablation [23]. In the case of osteoporotic vertebral body, sacral, and rib fractures, bisphosphonate treatment and vertebroplasty can be considered [23]. Degenerative lesions, if concordant with the symptoms, can be managed with percutaneous injections of anesthetics or corticosteroids. It has been proven that findings on bone scintigraphy are predictive of the short-term outcome of facet-joint injections in patients with lower back pain. It may be possible to use SPECT and, even better, SPECT/CT to differentiate costovertebral joint osteoarthritis and facet joint osteoarthritis and to guide therapeutic intervention [24-26].
Our study showed that digital fusion of bone SPECT and full-dose CT images is technically feasible. Correct anatomic fusion by bringing internal anatomic landmarks into agreement was possible for all patients. The disadvantage of this technique is that it is time consuming in the daily routine: It takes approximately 15 minutes to fuse images. The advantage is that the images also can be fused with CT data obtained at other institutions. There is no need to repeat CT studies if images of the relevant region are available in DICOM format. The clear advantage of an in-line SPECT/CT system is greater comfort for the patient because transfer from one scanner to another is not necessary. Obviation of transfer also results in faster imaging and postprocessing workflow. Römer et al. [8] recently reported data on cancer patients who underwent imaging with an inline SPECT/CT system. The authors found that SPECT-guided CT clarified most of the lesions. The 64-MDCT technique substantially improved noninvasive imaging of the coronary arteries, as has been shown in several publications [27].
To our knowledge, inline systems with a combination of SPECT and 64-MDCT are not available. On the other hand, the quality of 4- to 6-MDCT, which is available in combined scanners, seems sufficient for evaluation of bone lesions in the axial skeleton. In combined scanners, the CT data can be used for attenuation correction of the SPECT images. Attenuation correction with CT data from separate scanners also is feasible, as has been found in heart studies [28]. Most authorities consider MRI of scintigraphically indeterminate lesions of the axial skeleton the most appropriate examination. Compared with CT, MRI is more time consuming and more expensive, and contraindications such as severe claustrophobia and the presence of pacemaker implants have to be considered. Nevertheless, SPECT-guided MRI of indeterminate spinal lesions should be the first choice for imaging of young patients. Integrated SPECT/MRI scanners are not available, but our experience with software-fused SPECT/MRI fusion has shown that this approach is feasible for the axial skeleton.
Our study had limitations. Histologic confirmation was not available for all patients because we could not ethically justify obtaining histologic proof of the diagnosis of all lesions identified, especially the degenerative lesions. Nevertheless, we did our best to establish the reference standard by using histologic, additional MRI, and planar scintigraphic follow-up whenever possible. In addition, clinical follow-up was used as the reference standard in all cases.
In conclusion, the visibility of focal lesions in the axial skeleton is significantly better with SPECT and with SPECT fused with CT than with planar bone scintigraphy. Planar scintigraphy may suffice for differentiation of benign and malignant lesions of the axial skeleton, but SPECT fused with CT significantly increases the certainty of diagnosis and is the best tool for specific diagnosis.
Footnotes
Address correspondence to K. Strobel ([email protected]).
WEB This is a Web exclusive article.
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Submitted: September 13, 2006
Accepted: November 21, 2006
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