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DOI: 10.1148/radiol.2253011707
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(Radiology 2002;225:889-894.)
© RSNA, 2002

Technical Developments

Vertebral Metastases: Assessment with Apparent Diffusion Coefficient1

Andreas M. Herneth, MD, Marcel O. Philipp, MS, Jonathan Naude, MD, Martin Funovics, MD, Reinhard R. Beichel, PhD, Roland Bammer, PhD and Herwig Imhof, MD

1 From the Department of Radiology (A.M.H., M.O.P., M.F., H.I.) and Clinic for Radiation Therapy (J.N.), University of Vienna, AKH-Wien, 8F, Währinger Gürtel 18-20, A-1090 Vienna, Austria; Department for Digital Picture Analysis, University of Technology Graz, Austria (R.R.B.); and Lucas MRI Center, Stanford University School of Medicine, Palo Alto, Calif (R.B.). Received October 18, 2001; revision requested January 2, 2002; final revision received April 25; accepted April 30. Address correspondence to A.M.H. (e-mail: andreas.herneth@univie.ac.at).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 Materials and Methods
 Results
 Discussion
 REFERENCES
 
The authors evaluated the apparent diffusion coefficient (ADC) in the assessment of vertebral metastases and acute vertebral compression fractures in 22 patients with known or suspected vertebral metastases. On the basis of significantly (P < .03) different ADCs, vertebral metastases (0.69 x 10-3 mm2/sec) and pathologic compression fractures (0.65 x 10-3 mm2/sec) can be safely distinguished from vertebral bodies (1.66 x 10-3 mm2/sec) and benign compression fractures (1.62 x 10-3 mm2/sec). Thus, the use of ADCs may increase the specificity of magnetic resonance imaging in these patients.

© RSNA, 2002

Index terms: Magnetic resonance (MR), diffusion study, 30.12144 • Magnetic resonance (MR), echo planar, 30.121416, 30.12144 • Spine, MR, 30.121416, 30.12144 • Spine, secondary neoplasms, 30.33


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and Methods
 Results
 Discussion
 REFERENCES
 
Vertebral metastases are frequently observed in patients with cancer (1). Magnetic resonance (MR) imaging has evolved as the diagnostic method of choice in these patients because of its excellent tissue contrast on T1-weighted MR images (2,3). In the adult spine, this tissue contrast occurs after "yellow" bone marrow is replaced by hypercellular tissue or increased water content (4,5). Although this natural contrast is sensitive, the specificity of this characteristic is limited because of similar signal intensity (SI) changes in both neoplasia and benign conditions such as inflammation, degeneration, or posttraumatic edema (6,7). In elderly patients, this lack of specificity frequently leads to diagnostic problems because benign (osteoporosis, trauma) and pathologic (metastases, cancer) compression fractures are common, and accurate diagnosis is important for appropriate treatment and prognosis (8–10).

In these patients, the specificity of MR imaging may be increased with the use of diffusion-weighted MR imaging because it is suitable for probing the structure of a biologic tissue at a microscopic level well below the typical millimeter scale resolution of MR imaging (11). The concept behind diffusion-weighted MR imaging is that it exploits the random translational motion of water protons, which results in loss of signal as a result of phase dispersion of the spins, which is proportional to the underlying apparent diffusion coefficient (ADC) (6,11–13). In the presence of diffusion-hindering obstacles such as membranes, tight junctions, fibers, macromolecules, and cell organelles, this translational motion of water protons is hindered, which results in a decreased diffusion capacity. According to this concept, diffusion is hindered in tissues with densely accumulated cells, such as tumor tissue, which results in increased SI on diffusion-weighted MR images. This theory has been derived from theoretic and biologic models and has been supported by findings of in vitro studies, animal models, and recent publications (2,6,9,14–22).

However, T2 shine-through effects also contribute to the SI on diffusion-weighted MR images and may therefore resemble hindered diffusion (2,23,24). Moreover, the SI on diffusion-weighted MR images depends on the b factor, which is strongly influenced by hardware components, imaging parameters, and the pulse sequence itself (25). This dependency reduces the usefulness of diffusion-weighted MR imaging for comparisons between subsequent investigations (eg, follow-up studies, monitoring) or surveys from other imagers and institutions. Thus, quantitative analysis of diffusion effects is mandatory to obtain an unbiased and comparable parameter that reflects only the physical properties of the tissue of interest in terms of the random movement of molecules (23).

Diffusion-weighted MR imaging performed with Stejskal-Tanner–type sequences, such as echo-planar imaging, has been proposed as the imaging method of choice for quantitative analysis of diffusion-weighted MR images (6,15,24). Technical constraints, such as limited spatial resolution, sensitivity to eddy currents, local susceptibility gradients, and chemical shift, restricted the use of diffusion-weighted echo-planar imaging to the study of brain disease for many years (26–30). As a result of improvements in hardware components and the use of echo-planar imaging with navigated echoes, however, these constraints have been partially overcome (26,31,32).

The purpose of this prospectively designed study was to evaluate the role of quantitative analysis of diffusion-weighted MR images in the assessment of vertebral metastases and acute vertebral compression fractures by calculating the ADC from navigated diffusion-weighted interleaved echo-planar MR images.


   Materials and Methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 REFERENCES
 
Between June 1998 and December 1999, we prospectively investigated the spine of 22 consecutive patients (19 women and three men; age range, 44.7–90.3 years; median age, 57.8 years) who were referred for MR imaging of known or clinically suspected vertebral metastases and who agreed to volunteer for diffusion-weighted MR imaging. Written informed consent was obtained from all patients prior to imaging. According to our national and institutional guidelines for ethical review, institutional review board approval was not necessary since ionizing radiation, contrast media, and invasive techniques were not included in the study design. Of these 22 patients, 15 had a known primary tumor (breast carcinoma, n = 11; bronchus carcinoma, n = 2; thyroid carcinoma, n = 1; and hypernephroma, n = 1).

Both conventional and diffusion-weighted MR imaging were performed with a 1.0-T MR imaging unit (Gyroscan T10-NT; Philips, Best, the Netherlands) with a spine radio-frequency array coil (Philips). Vertebral metastases were diagnosed on the basis of findings at conventional radiography and/or computed tomography (CT), MR imaging, and scintigraphy (5,33–35). In the seven patients without evidence of vertebral metastases, the diagnosis was confirmed with follow-up MR imaging, which was performed at 3 months after the initial survey on the basis of the MR imaging criteria of Moulopoulos et al (34). A true pathologic confirmation of the diagnosis based on the national and institutional guidelines for ethical review was not achievable, which is a limitation of our study. However, the design of the current study, which is consistent with national and institutional ethical requirements, is analogous to the designs of similar studies in the literature (2,6,21,34).

In seven of the 22 patients, there were 14 acute vertebral compression fractures. Compression fractures were considered acute if they occurred within 4 weeks prior to presentation. According to imaging findings (conventional radiographs, CT scans, MR images) and follow-up MR images obtained at 3 months after the initial survey, seven of these fractures were of a pathologic nature (ie, metastatic) and seven were of a benign nature (ie, osteoporotic or traumatic). All 14 acute compression fractures were evaluated as a subgroup.

At our institution, the routine protocol for MR imaging of the spine in patients with known or suspected vertebral metastases consists of the following sequences: T1-weighted spin-echo imaging (500/14 [repetition time msec/echo time msec]), T2-weighted turbo spin-echo imaging (2,687/120, 18 gradient echoes per shot), and short inversion time inversion-recovery, or STIR, imaging (1,400/30/150 [inversion time msec]). These images were obtained in sagittal orientation to cover the segment of the spine with a known metastasis or where a metastasis was suspected.

In addition, diffusion-weighted images were acquired, in exactly the same plane and orientation used in the routine sequences, by using a navigated interleaved echo-planar imaging sequence with fat saturation (2,500/102; 13 gradient echoes per shot; two signals acquired; field of view of 250 x 250 mm; section thickness of 6 mm; intersection gap of 0.1 mm; and matrix of 128 x 128, which was zero filled and reconstructed to 256 x 256). A navigator echo was used to minimize artifacts caused by involuntary motion when diffusion-encoding gradients were turned on (32,36,37). The signal-to-noise ratio was increased by obtaining isotropically diffusion-weighted images after calculation of the geometric average from diffusion-weighted MR images with diffusion sensitizing along the left to right, anteroposterior, and section directions. For objective assessment of image quality, the signal-to-noise ratio of vertebral metastases was calculated according to the following ratio: SIvm/SDair, where SIvm is the SI of the vertebral metastases and SDair is the SD of the background noise. The duration of the diffusion-weighted sequence was 3 minutes 24 seconds.

For quantitative analysis of tissue-specific diffusion properties, the ADC was calculated from the slope of the semilog plot of the SI as a function of the b factor from two diffusion-weighted images, according to the following equation: ADC = log(SI1/SI2)/(b2 - b1), where SI1 and SI2 are the SIs of diffusion-weighted images obtained with two b values (b1 and b2, respectively) (38). The b values used in this study were determined by the imager gradient system (maximum, 10 mT/m), which resulted in b1 of 440 sec/mm2 and b2 of 880 sec/mm2. The ADC was calculated offline on a pixel-by-pixel basis from user-defined regions of interest with an average size of 51 mm2 (minimum, 27 mm2; maximum, 85 mm2). The regions of interest were drawn in consensus on diffusion-weighted MR images by two experienced radiologists (A.M.H., M.O.P.), who matched SI changes on the T1-weighted spin-echo MR images.

In each patient, all vertebral metastases and suspected vertebral bodies were investigated. Also in each patient, one vertebral body without pathologic SI on MR images was examined, and it served as an internal control. Overall, 46 vertebrae (vertebral metastases, n = 24; normal vertebrae, n = 22) were evaluated (cervical spine, n = 5; thoracic spine, n = 17; lumbar spine, n = 24). If a patient presented with one or more vertebral compression fractures, they were evaluated separately. The SI on diffusion-weighted echo-planar images of vertebral metastases and normal vertebrae was also quantified for comparison with data presented previously.

Statistical analysis was performed with a commercially available personal-computer–based statistic package (SYSTAT; SPSS, Chicago, Ill). Descriptive statistics showed a normal distribution and equal variance for the ADCs and SIs. For statistical analysis of differences in the ADCs and SIs of vertebral metastases and normal vertebrae, the unpaired Student t test with Bonferroni correction was used. For statistical analysis of differences in the ADCs and SIs in the subgroup of patients with acute vertebral compression fractures, a nonparametric test (Mann-Whitney U test) was performed. If a patient had multiple acute vertebral compression fractures, which could present a problem in statistical analysis, the ADCs of these fractures were pooled. For comparison of intraindividual differences in ADCs and SIs, the paired Student t test was used. A P value of less than .03 was considered to indicate a statistically significant difference. The data are presented as mean values plus or minus 1 SD.


   Results
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
Discussion
 REFERENCES
 
The mean ADCs of vertebral metastases and normal vertebrae were 0.69 x 10-3 mm2/sec ± 0.24 and 1.66 x 10-3 mm2/sec ± 0.38, respectively (Fig 1a). The difference between these two entities was statistically significant (P > .001; 95% CI: 0.59, 0.79 and 1.50, 1.83, respectively). The mean difference between the ADC of vertebral metastases and normal vertebrae in each patient (intraindividual difference) was 0.55 x 10-3 mm2/sec ± 0.24 (95% CI: 0.41, 0.69). These data are summarized in Table 1.



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  		Figure 1a. Box plots of the ADCs (a) in normal vertebrae (VBod) and vertebral metastases (VMet) and (b) in benign (benFX) and pathologic (pathFX) vertebral compression fractures. The horizontal lines are mean values, the boxes show minimum and maximum values, and the whiskers indicate plus or minus 2 SDs. Mean ADCs for the vertebral bodies and vertebral metastases are significantly different, and there is no overlap of absolute values.

 


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  		Figure 1b. Box plots of the ADCs (a) in normal vertebrae (VBod) and vertebral metastases (VMet) and (b) in benign (benFX) and pathologic (pathFX) vertebral compression fractures. The horizontal lines are mean values, the boxes show minimum and maximum values, and the whiskers indicate plus or minus 2 SDs. Mean ADCs for the vertebral bodies and vertebral metastases are significantly different, and there is no overlap of absolute values.

 

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  		TABLE 1. ADCs of Vertebral Metastases, Vertebral Bodies, and Benign and Pathologic Compression Fractures

 
The vertebral compression fractures had analogous ADCs with regard to their genesis (Fig 1b). The mean ADC of pathologic vertebral compression fractures was 0.71 x 10-3 mm2/sec ± 0.27, which was significantly lower (probability: P < .03, z = -2.12, {chi}2 approximation = 4.5 with 1 degree of freedom) than the ADC in benign vertebral compression fractures of 1.61 x 10-3 mm2/sec ± 0.37. The 95% CIs for pathologic and benign vertebral compression fractures were 0.41, 0.89 and 1.24, 2.00, respectively. These data are also summarized in Table 1.

The mean SIs of the two differently sensitized diffusion-weighted MR images are summarized in Table 2. The SIs of vertebral metastases and normal vertebrae were significantly different (P < .0002), and the 95% CIs showed no overlap (Fig 2). However, the mean SIs of pathologic and benign vertebral compression fractures were not significantly different, and the 95% CIs overlapped substantially (Fig 3).


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  		TABLE 2. SIs of Vertebral Metastases, Vertebral Bodies, and Benign and Pathologic Compression Fractures on Diffusion-Weighted Echo-planar MR Images

 


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  		Figure 2. Sagittal MR images of the lower thoracic and upper lumbar spine in a 63-year-old woman with breast cancer, known vertebral metastasis at L1 (arrows), and acute pathologic compression fractures at T11 and T12 (arrowheads). Vertebral compression fractures are (A) hypointense on T1-weighted MR image (500/14) and (B) hyperintense on T2-weighted MR image (2,687/120). On diffusion-weighted echo-planar images (C, b value of 440 sec/mm2; D, b value of 880 sec/mm2), the vertebral metastasis and vertebral compression fractures appear hyperintense. E, ADC map shows both vertebral metastasis and acute pathologic vertebral compression fractures with low ADCs, which indicate hindered diffusion of water protons and the pathologic nature of these findings. Note the hyperintense area located centrally in the fracture of L1, which possibly indicates unhindered diffusion in an area of debris.

 


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  		Figure 3. Sagittal MR images of the thoracic spine in a 57-year-old woman with lung cancer and an acute vertebral compression fracture (T6) following trauma. The benign vertebral compression fracture (arrows) is (A) hypointense on T1-weighted spin-echo image (500/14) and (B) hyperintense on short inversion time inversion-recovery image (1,400/30/150) as a result of replacement of fatty bone marrow by edema. On diffusion-weighted echo-planar MR images (C, b value of 440 sec/mm2; D, b value of 880 sec/mm2), this area appears hyperintense as a result of T2 shine-through effects. E, ADC map shows high ADCs as a result of the unhindered mobility of water protons, which indicates the benign nature of the acute vertebral compression fracture. The diagnosis was confirmed at follow-up MR imaging, which was performed at 3 months after the initial survey (34). Note the hyperintense area located centrally in the fracture of L1, which possibly indicates unhindered diffusion in an area of debris. Analogous SI changes (arrowheads) can be seen in the ventral portion of T7 and the dorsal portion of T8, which indicates posttraumatic edema.

 
On diffusion-weighted MR images obtained with a b value of 880 sec/mm2, the signal-to-noise ratios for vertebral metastases and normal vertebrae were 27.6 and 9.1, respectively, which provided sufficient contrast for reliable quantitative analysis of diffusion effects and SIs (Figs 2, D; 3, D).


   Discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
REFERENCES
 
Baur and colleagues (7,21) introduced diffusion-weighted MR imaging as a noninvasive technique with which to distinguish pathologic from benign vertebral compression fractures by revealing differences in SIs. They visually assessed SI changes on diffusion-weighted MR images by using a steady-state free precession technique. However, this technique seems to have no advantage over conventional MR imaging with regard to detection and characterization of compression fractures (2). As indicated by several authors, this limitation may be caused by confounding relaxation phenomena, so-called T2 shine-through effects, and perfusion effects that may mask diffusion-related SI patterns (6,11,23,24,39). Results of SI quantification, as presented in the current study, support this hypothesis. On diffusion-weighted MR images, the SIs of pathologic acute vertebral compression fractures were significantly higher than those of benign acute vertebral compression fractures, but the absolute values and the 95% CIs of these two entities showed substantial overlap. This finding reduces the usefulness of this technique.

As claimed by various authors, quantitative analysis of diffusion effects, which can be achieved by calculating the ADC, is mandatory to eliminate these interfering effects (6,23,24). In the current study, quantitative analysis of diffusion effects was accomplished by calculating the ADC from navigated diffusion-weighted interleaved echo-planar MR images. The ADC of normal vertebrae was significantly higher than that of vertebral metastases, which supports the hypothesis that water mobility in tumors is hindered. The good reliability of the ADC in the assessment of vertebral metastases is characterized by the differences in the mean values and the clearly separated CIs. Thus, the ADC is a dependable and quantifiable parameter with which to distinguish normal vertebrae from vertebral metastases. Because the ADC is a quantitative parameter, it might be used for monitoring of treatment by revealing treatment-related changes in tissue characteristics (40). This aspect, however, was beyond the scope of the current study.

The ADCs of the acute vertebral compression fractures were analogous to those of normal vertebrae and vertebral metastases with regard to their nature. Although the absolute ADCs in this subgroup were similar to those of the general study population, the differences in the ADCs yielded less significance. This finding can be explained by the fact that the subgroup was smaller than the general study population and that patients with multiple fractures were evaluated, which may present problems in statistical analysis. To overcome these problems, the data for patients with multiple acute compression fractures were pooled and a nonparametric test was used. Thus, by taking into account that the 95% CIs of the ADCs were discrete and the differences in the ADCs were significant, the ADC seems to be a useful tool with which to increase the specificity of MR imaging in the characterization of acute vertebral compression fractures.

The ADCs of normal vertebrae in the current study are higher than those reported by Dietrich et al (18), who calculated the ADC of the cervical spine in six healthy volunteers. This difference may be a result of MR signals from yellow bone marrow, which come primarily from lipid-bound protons and are conceivably less mobile than are unbound protons (ie, free water). Since echo-planar imaging methods are susceptible to resonance offsets, such as the water-fat shift, we applied fat saturation to the diffusion-weighted sequence used in this study. Although the application of fat saturation reduces the signal-to-noise ratio in normal vertebrae according to the low abundance of unbound protons, we achieved sufficient image quality for quantitative diffusion analysis. The ADCs derived from these images are comparable to those of tissues with low fat content, such as the brain, spinal cord, and kidneys, and head and neck lesions (18,28,41,42).

ADC maps could not be generated at the time that the current study was performed because the software version of the imager was unable to calculate the ADC with a pixel-by-pixel method. However, ADC maps were generated offline for presentation purposes after the study was completed. Areas with low SIs reflect hindered diffusion, as is apparent in vertebral metastases and in pathologic vertebral compression fractures. Normal vertebrae appear hyperintense on ADC maps; this finding indicates nonhindered diffusion. In normal vertebrae, however, black areas may occur beside hyperintense areas, which may affect visual interpretation. As can be seen on the corresponding diffusion-weighted MR images and T1-weighted images, these areas reflect tissue compartments without signals, such as calcified bone (eg, trabeculae, cortex), or are the result of fat saturation. Thus, quantitative analysis of diffusion-weighted MR images on a pixel-by-pixel basis is preferable to the visual assessment of ADC maps. However, this difference may not apply for tissues with a high content of unbound water protons, such as tumor or posttraumatic edema.

In conclusion, navigated diffusion-weighted interleaved echo-planar MR imaging of the spine is feasible for quantitative analysis of diffusion effects, and the ADC calculated from diffusion-weighted MR images is a reliable parameter with which to distinguish vertebral metastases from normal vertebrae. Furthermore, the ADC promises to be a potential tool for characterization of acute vertebral compression fractures, which may increase the diagnostic potential and safety of MR imaging in the assessment of spinal lesions.


   ACKNOWLEDGMENTS
 
The authors thank Jack Van der Kooi for his help regarding technical aspects in diffusion-weighted MR imaging and for preparing the MR images for this article.


   FOOTNOTES
 
Abbreviations: ADC = apparent diffusion coefficient, SI = signal intensity

Author contributions: Guarantor of integrity of entire study, A.M.H.; study concepts and design, A.M.H., H.I.; literature research, M.O.P., M.F.; clinical studies, A.M.H., J.N.; data acquisition, A.M.H., M.F., M.O.P.; data analysis/interpretation, A.M.H., M.F.; statistical analysis, A.M.H., M.O.P.; manuscript preparation, M.O.P., A.M.H.; manuscript definition of intellectual content, A.M.H., R.B.; manuscript editing, M.F.; manuscript revision/review, H.I., R.B.; manuscript final version approval, H.I., A.M.H.


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 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
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