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Musculoskeletal Imaging |
1 From the Departments of Clinical Radiology (A.B., A.S., M.R.), Pathology (S.A.), Orthopedic Surgery (H.R.D.), and Internal Medicine (R.B.), University of MunichGrosshadern, Marchioninistrasse 15, 81377 Munich, Germany. Received August 20, 2001; revision requested September 24; final revision received April 29, 2002; accepted May 16. Address correspondence to A.B. (e-mail: andrea.baur@ikra.med.uni-muenchen.de).
| ABSTRACT |
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MATERIALS AND METHODS: The study group comprised 87 consecutive patients with acute vertebral compression fractures due to osteoporotic (n = 52) or neoplastic (n = 35) infiltration. The MR imaging protocol included nonenhanced T1-weighted spin-echo and short inversion time inversion-recovery sequences and a 1.5-T system. Readers blinded to the outcome documented the occurrence, shape, and location of the fluid sign with consensus. The fluid sign was correlated with the cause, age, and severity of the fracture. The diagnosis was confirmed with surgery, follow-up MR imaging, clinical follow-up, or unequivocal imaging findings. Wilcoxon and
2 tests were used to assess significance.
RESULTS: In fractured vertebral bodies, the fluid sign was adjacent to the fractured end plates and exhibited signal intensity isointense to that of cerebrospinal fluid. The fluid sign was linear (n = 16), triangular (n = 5), or focal (n = 2) and was significantly associated with osteoporotic fractures (21 [40%] of 52; P < .001). The fluid sign occurred in two (6%) of 35 neoplastic compression fractures. Histologic examination demonstrated osteonecrosis, edema, and fibrosis at the site of the fluid sign. There was a tendency toward older fractures exhibiting the fluid sign, but this relationship was not significant (P > .05). In osteoporotic fractures, the fluid sign was significantly associated with fracture severity (P < .05).
CONCLUSION: The fluid sign is featured in acute vertebral compression fractures that show bone marrow edema. It can be an additional sign of osteoporosis and rarely occurs in metastatic fractures.
© RSNA, 2002
Index terms: Osteoporosis, 30.56 Spine, fractures, 30.411 Spine, MR, 30.121411, 30.121413 Spine, secondary neoplasms, 30.33
| INTRODUCTION |
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Magnetic resonance (MR) imaging has proved useful in the distinction of osteoporotic from malignant fractures (13). Morphologic signs such as the degree and pattern of bone marrow replacement, paravertebral soft-tissue masses, and infiltration of posterior elements of the vertebrae are signs for assessing the cause of the fracture. Also, diffusion-weighted imaging has been shown to aid in establishing the correct diagnosis (57). At MR imaging, the presence of a fluid collection has been described in rare cases of avascular necrosis of the vertebral body (8,9). The purpose of our study was to evaluate the occurrence, location, and shape of the fluid sign, or fluid collection, in acute osteoporotic and neoplastic vertebral compression fractures at MR imaging.
| MATERIALS AND METHODS |
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The diagnosis was confirmed by means of surgery in 26 patients, follow-up MR imaging in 23, clinical follow-up in 24, and unequivocal imaging findings in 14. Direct histologic comparison was performed in four patients in whom a ventrodorsal surgical approach was used. In patients in whom follow-up MR imaging was used to confirm the diagnosis, the disappearance of bone marrow edema and restitution of fat cells in the fractured vertebral bodies were used to prove the benign nature of the vertebral fracture. Follow-up MR imaging was performed 413 months after the study MR imaging. Clinical follow-up was performed 812 months after the initial fracture and comprised physical examination and radiography. The relief of pain and lack of vertebral destruction were used to confirm the benign nature of a fracture. Paravertebral soft-tissue extension, infiltration of posterior elements, and presence of multiple metastases to the remainder of the vertebral column were considered unequivocal imaging findings for a neoplastic fracture.
Thus, 52 patients (41 women, 11 men; age range, 3487 years; mean age, 68 years) with 65 vertebral compression fractures due to osteoporosis and 35 patients (20 women, 15 men; age range, 3384 years; mean age, 62 years) with 41 vertebral compression fractures due to tumor were identified. Underlying malignancies in the group with malignant fractures included breast cancer (n = 13), multiple myeloma (n = 4), bronchogenic carcinoma (n = 3), adenocarcinoma of unknown primary cause (n = 3), renal cell carcinoma (n = 2), pancreatic cancer (n = 2), prostate cancer (n = 2), transitional cell carcinoma (n = 2), colon carcinoma (n = 1), stomach cancer (n = 1), carcinoma of the urinary bladder (n = 1), and thyroid cancer (n = 1).
Our institutional review board did not require its approval for our study. Since the standard clinical work-up in patients with unclear vertebral fractures is MR imaging, a special informed consent form was not required by our institutional review board. The patients were informed according to the standard information form for MR imaging. Patients with metal implants or cardiac pacemakers were excluded.
Imaging
MR imaging was performed with a 1.5-T system (Vision; Siemens, Erlangen, Germany) by using a spine-array surface coil. The imaging protocol included sagittal T1-weighted spin-echo images (450648/1215 [repetition time msec/echo time msec]) and short inversion time inversion-recovery (STIR) images (3,600/60/150 [inversion time msec]) with 4-mm section thickness. The matrix was 256 x 512, with a field of view of 500 mm.
Image Review
Two experienced radiologists (A.S., M.R.) qualitatively evaluated the vertebral fractures on the T1-weighted spin-echo and STIR images for the extent of bone marrow replacement. The reading was performed in consensus, and the radiologists were blinded to the results. The extent of bone marrow alteration on T1-weighted spin-echo images was diagnosed as bandlike when it was adjacent to the end plate, as incomplete when some islands of fat were still present in the fractured vertebral body, and as complete when the entire bone marrow of the fractured vertebral body was involved.
The presence or absence of the fluid sign was assessed. The fluid sign was defined as a focal, linear, or triangular area of strong hyperintensity on STIR images on a background of diffuse hyperintensity in the vertebral body because of acute collapse. The signal intensity of the fluid sign had to be equivalent to that of cerebrospinal fluid. The location of the fluid sign was evaluated.
Statistical Analysis
The
2 test was used to determine whether the occurrence of the fluid sign in the two groups, as well as the occurrence of the fluid sign and the severity of the fracture (bone marrow edema), was significant. The relationship between the age of the fracture and the occurrence of the fluid sign was tested by means of the Wilcoxon rank sum test. Thirteen patients had several fractures at the same time. Because of statistical independence problems, one fracture was chosen for each patient by means of a randomization procedure. Statistical significance was assumed at a P value less than .05.
| RESULTS |
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The fluid sign was detected in 23 (26%) of 87 fractures. In vertebral fractures due to osteoporosis, the fluid sign was apparent in 21 (40%) of 52 cases (Figs 13). In vertebral fractures due to tumor, the fluid sign was found in two (6%) of 35 cases (Fig 4). The underlying malignancy was bronchogenic carcinoma in the first case and breast cancer in the second. This difference in the frequency of the fluid sign was significant (P < .001).
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2 test, P = .22). In the osteoporotic fractures, the fluid sign was linear in 15, triangular in four, and focal on several consecutive sagittal sections in two. This latter pattern represented a linear left-to-right direction of the fluid. The linear extension would have been better shown on coronal sections; however, those were not obtained. In the two malignant fractures, the fluid was triangular in one case (Fig 4) and linear in the other.
The fluid sign was located adjacent to the superior end plate in 16 cases and to the inferior end plate in five. It was located in the anterior aspect of the vertebral body in 20 cases, posteriorly in one, and centrally in two. Association of the presence of the fluid sign with the age of the fracture was not significant, although there was a tendency for fractures that exhibited the sign to be slightly older (Wilcoxon test, P > .05).
Histologic comparison of the fluid sign was performed in four osteoporotic and one metastatic fracture. Surgery was performed ventrodorsally in these patients, and the vertebral bodies were replaced by metallic cages. The remainder of the patients who had osteoporosis and underwent surgery had a dorsal or dorsolateral surgical approach with only bone marrow biopsy results from the vertebral body to exclude tumor. Therefore these patients did not have comparison with the region that exhibited the fluid sign. The second patient with malignancy that exhibited the fluid sign had multiple metastases to the spine because of breast cancer, so primary radiation therapy was started. Thus, in that patient, histologic examination of the region that exhibited the fluid sign was not attempted.
In all four patients with osteoporosis, histologic examination results showed necrotic bone in the area of the fluid sign. In two patients, circumscribed areas of bone marrow necrosis were present at the site of the fluid sign. Normal bone marrow with hematopoietic cells and fat cells was nearly completely replaced by bone marrow edema and reactive fibrosis. Increased amounts of osteoclasts and osteoblasts surrounded the trabecular network. In the neoplastic fracture, dense tumor cell infiltration due to a poorly differentiated adenocarcinoma was present. At the site of the fluid sign, in the anterior part of the wedge-shaped fracture, osteonecrotic bone and necrotic bone marrow without tumor cell infiltration were seen (Fig 4). Tumor search with computed tomography (CT) revealed bronchogenic carcinoma as the underlying cause.
| DISCUSSION |
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However, the absence of these findings does not exclude a malignant fracture. In a series of 53 patients, Baker et al (3) found that acute benign fractures more often show inhomogeneous low signal intensity on T1-weighted spin-echo and fat-suppressed images and inhomogeneous high signal intensity on T2-weighted and STIR images. In contrast, pathologic fractures showed more homogeneous replacement of the bone marrow, which reflects diffuse bone marrow replacement by tumor cells. Similarly, Yuh et al (2) found that complete loss of signal intensity in the bone marrow on T1-weighted images provides a high level of accuracy in diagnosis of malignant fractures. Benign fractures showed incomplete replacement of bone marrow. In chronic compression fractures, fat signal intensity was preserved.
At MR imaging, the fluid sign has been described in rare cases of avascular necrosis of the vertebral body (8,9). Naul et al (8) examined five patients with avascular necrosis of the vertebral body diagnosed at radiography. Similar to findings in the patients with osteoporotic and pathologic vertebral compression fractures in our study, a circumscribed fluidlike signal intensity was present adjacent to the end plate on T2-weighted spin-echo images. Histologic analysis of a biopsy specimen showed signs of reactive marrow fibrosis with high bone turnover, osteoclasts, and osteoblasts, which were nonspecific but indicative of osteonecrosis.
Dupuy et al (9) reported three cases of avascular necrosis of vertebral bodies that showed more extensive fluid accumulation. The fluid accumulation made up a large amount of the vertebral body and appeared as a smoothly marginated region of strong hyperintensity on T2-weighted images. With a CT-guided procedure, fluid could be aspirated. Histologic analysis of core biopsy specimens showed small fragments of bone and fibrosis.
In the series of Naul et al (8) and Dupuy et al (9), the fractures showed an intravertebral vacuum at radiography. In our study, only two fractures exhibited an intravertebral vacuum at radiography. At CT, the incidence would probably be higher, since CT is more sensitive in depicting air (10).
Until the writing of this article, to our knowledge, no prior articles described the prevalence of the fluid sign in acute osteoporotic and pathologic vertebral compression fractures at MR imaging. We have shown that the fluid sign is a common finding in acute and subacute vertebral fractures, and it occurred in 26% of all fractures in our series. The fluid sign is indicative of the acute benign osteoporotic cause of a fracture, with 40% of these fractures showing this sign (Figs 13).
To our knowledge, the fluid sign has not been described in MR studies of tumorous fractures. In our series, two malignant fractures (6%) also demonstrated the fluid sign. Comparison with histologic examination results in one malignant fracture showed incomplete infiltration of the vertebral body with tumor next to osteonecrosis without tumor cells in the anterior part that exhibited the fluid sign.
The pathogenesis of osteonecrosis in a vertebral body is twofold. The first mechanism is that of avascular necrosis, known as Kümmel disease (11). Kümmel described delayed vertebral collapse in laborers. This concept was supported by Schmorl and Junghanns (12) on the basis of vertebral specimens. Authors of two case reports (13,14) showed delayed vertebral collapse due to osteonecrosis. With sequential radiography and scintigraphy, these authors were able to confirm at radiography that no fracture was present at the time of trauma. The mechanism is believed to represent trauma-induced osteonecrosis of a vertebral body with subsequent collapse in the presence of predisposing factors such as arteriosclerosis (15).
The second cause of osteonecrosis in a vertebral body are vertebral fractures arising secondary to bone weakness in patients with osteoporosis in conjunction with minor trauma or because of tumor in metastatic disease. Thus, osteoporosis and minor trauma result in a vertebral fracture, and osteonecrosis develops at the site of the fractured end plate because of strong compression of the trabecular network in that area. The fluid sign always occurred at the site of the fractured end plate, where compression of the spongiosa was most severe. The fluid sign did not occur in fractures with only minor damage represented by the fractures with only bandlike bone marrow edema. We propose that in acute osteoporotic fractures with bone marrow edema, fluid is pressed into the space of osteonecrosis and causes the fluid sign at MR imaging. In rare cases, the fluid sign can also occur in tumorous fractures.
The reason why osteonecrosis or a vacuum is associated with the benign nature of a fracture might be twofold. First, in a tumorous fracture the vertebral body is filled with tumor cells. Second, osteoporosis is an underlying factor for the development of osteonecrosis in case the vertebral body fractures. Staebler et al (10) found an inverse correlation between the presence of an intravertebral vacuum and bone mineral density in vertebral compression fractures.
In conclusion, the fluid sign at MR imaging may be regarded as an additional morphologic feature that supports the benign osteoporotic nature of an acute fracture. Although this finding is significant, a tumor cannot be excluded because of this sign. Other morphologic features or diffusion-weighted imaging should be considered if the diagnostic decision is difficult.
| FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, A.B.; study concepts, A.B., A.S.; study design, A.B., M.R.; literature research, A.S., H.R.D.; clinical studies, H.R.D.; data acquisition, A.B., S.A.; data analysis/interpretation, R.B., A.B.; statistical analysis, A.B., H.R.D.; manuscript preparation, A.B.; manuscript definition of intellectual content, A.B., A.S., M.R.; manuscript revision/review, M.R.; manuscript editing and final version approval, A.B., A.S.
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