Acute Osteoporotic and Neoplastic Vertebral Compression Fractures: Fluid Sign at MR Imaging 1

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1 Musculoskeletal Imaging Radiology Andrea Baur, MD Axel Stäbler, MD Susanne Arbogast, MD Hans Roland Duerr, MD Reiner Bartl, MD Maximilian Reiser, MD Index terms: Osteoporosis, Spine, fractures, Spine, MR, , Spine, secondary neoplasms, Published online before print /radiol Radiology 2002; 225: Abbreviation: STIR short inversion time inversion recovery 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 Munich Grosshadern, Marchioninistrasse 15, Munich, Germany. Received August 20, 2001; revision requested September 24; final revision received April 29, 2002; accepted May 16. Address correspondence to A.B. ( andrea.baur@ikra.med.uni -muenchen.de). Acute Osteoporotic and Neoplastic Vertebral Compression Fractures: Fluid Sign at MR Imaging 1 PURPOSE: To evaluate the occurrence, location, and shape of the fluid sign in acute osteoporotic and neoplastic vertebral compression fractures at magnetic resonance (MR) imaging. 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 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. RSNA, 2002 Acute vertebral compression fractures are common and may occur because of trauma, osteoporosis, or neoplastic infiltration in a vertebral body. Although trauma does not pose a diagnostic problem, the determination of the benign or malignant causes of vertebral compression fractures may be challenging (1 4). Particularly in the elderly population, a neoplastic fracture may represent the first manifestation of a malignancy. On the other hand, osteoporosis is common, and vertebral fractures may occur even without trauma or after minor trauma. Magnetic resonance (MR) imaging has proved useful in the distinction of osteoporotic from malignant fractures (1 3). 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, diffusionweighted imaging has been shown to aid in establishing the correct diagnosis (5 7). 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. 730

2 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 4 13 months after the study MR imaging. Clinical follow-up was performed 8 12 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, years; mean age, 68 years) with 65 vertebral compression fractures due to osteoporosis and 35 patients (20 women, 15 men; age range, 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 Figure 1. MR images obtained in a 76-year-old woman with acute collapse of the fourth lumbar vertebral body because of osteoporosis. (a) Sagittal T1-weighted spin-echo image (450/12, 4-mm section thickness) shows complete hypointensity in the vertebral body. (b) Sagittal STIR image (3,600/60/150) shows diffuse hyperintensity in the fractured vertebral body because of bone marrow edema. Anteriorly and adjacent to the fractured superior end plate, a linear area of hyperintensity, isointense to cerebrospinal fluid, can be delineated on the STIR image. This represents the fluid sign (arrow). MATERIALS AND METHODS Patients The study group comprised 87 consecutive patients who were referred for MR imaging to evaluate acute vertebral collapse that was diagnosed at radiography. Inclusion criteria were fractures that occurred without trauma or with minor trauma (eg, fall from standing height). Patients with severe trauma (eg, due to a car accident) were not included. Radiography was performed 1 day to 1 week (mean, 3 days) after onset of symptoms. MR imaging was performed 1 40 days (mean, 15 days) after radiography. All patients had pain at the site of fracture; 55 patients complained of leg weakness. 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 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 ( /12 15 [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 , 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 spinecho 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 Volume 225 Number 3 Acute Osteoporotic and Neoplastic Vertebral Compression Fractures: MR Imaging 731

3 Figure 2. MR images obtained in a 61-year-old woman with a spontaneous fracture of the fourth lumbar vertebral body. The patient had chronic hepatitis C, and a tumor was suspected. (a) Sagittal T1-weighted spin-echo image (450/15, 4-mm section thickness) shows complete bone marrow replacement. (b, c) Sagittal STIR images (3,600/60/150) show hyperintensity in the fractured vertebral body and posterior bulging into the spinal canal. Adjacent to the fractured upper end plate is a focal area of fluidlike hyperintensity representing the fluid sign (arrow). It was displayed on several consecutive sections. However, surgery was performed, and histologic results showed the benign nature of the fracture. 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 All fractures showed hypointensity on T1-weighted spin-echo images and hyperintensity on STIR images, which is indicative of an acute fracture. Of the 52 benign osteoporotic fractures, bone marrow edema was bandlike in six, incomplete in 23, and complete in 23. In the 35 malignant fractures, bone marrow replacement was incomplete in two and complete in 33. The benign vertebral fractures occurred from the fifth thoracic to the fifth lumbar vertebral body, with 24 fractures in the thoracic spine and 28 in the lumbar spine. The neoplastic vertebral fractures occurred from the fourth cervical to the fifth lumbar vertebral body, with three in the cervical spine, 23 in the thoracic spine, and nine in the lumbar spine. At radiography, two osteoporotic vertebral fractures showed intravertebral air. 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 1 3). 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). In the osteoporotic group, the fluid sign was present in 13 of the 23 fractures that showed complete bone marrow replacement and in eight of the 23 fractures with incomplete bone marrow edema. No fluid sign was found in fractures with bandlike bone marrow edema. A significant association was found between the severity of the fracture and the occurrence of the fluid sign in the osteoporotic group (P.05). However, association between the fluid sign and the severity of the fracture was no longer significant when the tumorous fractures were included, which indicates a different pathologic mechanism ( 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). 732 Radiology December 2002 Baur et al

4 Figure 3. MR images obtained in a 66-year-old woman who had fallen from standing height and had an osteoporotic fracture of the 11th thoracic vertebral body. (a) Sagittal T1-weighted spinecho image (450/15, 4-mm section thickness) shows complete bone marrow replacement due to edema. (b) Sagittal STIR image (3,600/60/150) shows hyperintensity and a linear fluid sign (arrow) at the fractured lower end plate of the vertebral body. 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 The differentiation between acute benign osteoporotic and neoplastic vertebral collapse is a common problem in clinical radiology. Establishing the correct diagnosis is of great importance in determining treatment, surgical approach, and prognosis. T1- and T2-weighted sequences without or with fat saturation show similar signal intensities for both benign osteoporotic and neoplastic fractures. Thus, the morphology of bone marrow replacement has been evaluated for prediction of the benign or pathologic cause of a fracture. Paravertebral soft-tissue masses and infiltration of posterior elements are the most reliable signs of a malignant fracture (1). 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 Volume 225 Number 3 Acute Osteoporotic and Neoplastic Vertebral Compression Fractures: MR Imaging 733

5 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 1 3). 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 Figure 4. Images obtained in a 70-year-old man with an acute collapse of the 12th thoracic vertebral body. (a) Sagittal T1-weighted spin-echo MR image (450/15, 4-mm section thickness) shows complete hypointensity. (b) STIR image (3,600/ 60/150) shows hyperintensity. The vertebral collapse was due to metastatic bronchogenic carcinoma. Similar to findings in the osteoporotic fractures, a triangular fluid sign (arrow) was apparent in the anterior part of the fractured vertebral body on STIR images. (c) Photomicrograph from the anterior portion of the fractured vertebral body shows necrotic bone (thin arrows) and necrotic bone marrow (thick arrows) without infiltrating tumor. (Hematoxylin-eosin stain; original magnification, 200.) 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. References 1. Resnick D, Niwayama G. Osteoporosis. In: Resnick D, ed. Diagnosis of bone and joint disorders. 3rd ed. Philadelphia, Pa: Saunders, 1995; Yuh WTC, Zachar CK, Barloon TJ, Sato Y, Sickels WJ, Hawes DR. Vertebral compression fractures: distinction between benign and malignant causes with MR imaging. Radiology 1989; 172: Baker LL, Goodman SB, Perkash I, Lane B, Enzmann DR. Benign versus pathologic compression fractures of vertebral bodies: assessment with conventional spin-echo, 734 Radiology December 2002 Baur et al

6 chemical shift, and STIR MR imaging. Radiology 1990; 174: Frager D, Elkin C, Swerdlow M, Bloch S. Subacute osteoporotic compression fractures: misleading magnetic resonance appearance. Skeletal Radiol 1988; 17: Baur A, Stäbler A, Brüning R, et al. Diffusion-weighted MR imaging of bone marrow: differentiation of benign versus pathologic vertebral compression fractures. Radiology 1998; 207: Baur A, Huber A, Ertl-Wagner B, et al. Diagnostic value of increased diffusionweighting of a steady-state free precession sequence for the differentiation of acute benign osteoporotic versus pathologic vertebral compression fractures. AJNR Am J Neuroradiol 2001; 22: Spüntrup E, Buecker A, Adam G, van Vaals J, Günther RW. Diffusion-weighted MR imaging for differentiation of benign fracture edema and tumor infiltration of the vertebral body. AJR Am J Roentgenol 2001; 176: Naul LG, Peet GJ, Maupin WB. Avascular necrosis of the vertebral body. Radiology 1989; 172: Dupuy DE, Palmer WE, Rosenthal DI. Vertebral fluid collection associated with vertebral collapse. AJR Am J Roentgenol 1996; 167: Staebler A, Schneider P, Link TM, et al. Intravertebral vacuum phenomenon following fractures: CT study on frequency and etiology. J Comput Assisst Tomogr 1999; 23: Kümmel H. Die rarefizierende osteitis der wirbelkörper. Dt Med 1895; 21: Schmorl G, Junghanns H. The human spine in health and disease. 2nd ed. New York, NY: Grune & Stratton, 1971; Brower AC, Downey EF. Kümmel disease: report of a case with serial radiographs. Radiology 1981; 141: Van Eenenaam DP, El-Khoury GY. Delayed vertebral collapse (Kummel s disease): case report with serial radiographs, computed tomographic scans and bone scans. Spine 1993; 18: Stojanovic J, Kovac V. Diagnosis of ischemic vertebral collapse using selective spinal angiography. Rofo Fortschr Geb Rontgenstr Neuen Bildgeb Verfahr 1981; 135: Volume 225 Number 3 Acute Osteoporotic and Neoplastic Vertebral Compression Fractures: MR Imaging 735