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Neuroradiology |
1 From the Departments of Radiology (M.L., S.C., E.A.K., G.J., J.A., A.W.L.) and Neurosurgery (E.A.K.), NYU Medical Center, 560 First Ave, RIM Rm 234, New York, NY 10016. From the 2000 RSNA scientific assembly. M.L. supported by a 2000 RSNA Fellow Research Trainee Prize and a grant from the Royal Australian and New Zealand College of Radiologists. S.C. supported by an RSNA Seed Grant. Received March 5, 2001; revision requested April 12; revision received July 9; accepted August 15. Address correspondence to M.L. (e-mail: lawm01@med.nyu.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Fifty-one patients with a solitary brain tumor (33 gliomas, 18 metastases) underwent conventional, contrast material–enhanced perfusion-weighted, and proton spectroscopic MR imaging before surgical resection or stereotactic biopsy. Of the 33 patients with gliomas, 22 underwent perfusion-weighted MR imaging; nine, spectroscopic MR imaging; and two underwent both. Of the 18 patients with metastases, 12 underwent perfusion-weighted MR imaging, and six, spectroscopic MR imaging. The peritumoral region was defined as the area in the white matter immediately adjacent to the enhancing (hyperintense on T2-weighted images, but not enhancing on postcontrast T1-weighted images) portion of the tumor. Relative cerebral blood volumes in these regions were calculated from perfusion-weighted MR data. Spectra from the enhancing tumor, the peritumoral region, and normal brain were obtained from the two-dimensional spectroscopic MR acquisition. The Student t test was used to determine if there was a statistically significant difference in relative cerebral blood volume and metabolic ratios between high-grade gliomas and metastases.
RESULTS: The measured relative cerebral blood volumes in the peritumoral region in high-grade gliomas and metastases were 1.31 ± 0.97 (mean ± SD) and 0.39 ± 0.19, respectively. The difference was statistically significant (P < .001). Spectroscopic imaging demonstrated elevated choline levels (choline-to-creatine ratio was 2.28 ± 1.24) in the peritumoral region of gliomas but not in metastases (choline-to-creatine ratio was 0.76 ± 0.23). The difference was statistically significant (P = .001).
CONCLUSION: Although conventional MR imaging characteristics of solitary metastases and primary high-grade gliomas may sometimes be similar, perfusion-weighted and spectroscopic MR imaging enable distinction between the two.
© RSNA, 2002
Index terms: Brain neoplasms, diagnosis, 13.363, 13.3634, 13.38 • Brain neoplasms, MR, 13.121412, 13.121415, 13.121416, 13.12143, 13.12144, 13.12145 • Brain neoplasms, secondary, 13.38 • Magnetic resonance (MR), spectroscopy, 13.12144, 13.12145 • Magnetic resonance (MR), perfusion study, 13.12144, 13.12145
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Investigators in several studies (1–5) have used single-voxel MR spectroscopy and multivoxel metabolic mapping techniques in an attempt to differentiate the two entities. However, the conclusion each time has been that proton spectroscopic MR imaging cannot be used to reliably discriminate between metastases and primary brain tumors. In most of these studies, investigators compared spectra from only the enhancing portion of the lesion. To our knowledge, no researchers have investigated the region adjacent to the enhancing tumor, the so-called peritumoral region, which demonstrates signal abnormality at T2-weighted MR imaging. Spectroscopic MR imaging is now readily available and allows simultaneous acquisition of spectra from the enhancing portion of a tumor, the peritumoral region, and normal contralateral brain tissue.
At pathologic examination, peritumoral signal abnormality represents a tumor-induced increase in interstitial water due to alterations in capillary permeability and blood-brain barrier breakdown. In primary high-grade gliomas, peritumoral areas demonstrate not only altered capillary morphologic findings and interstitial water but also scattered tumor cells infiltrating along newly formed or preexisting but dilated vascular channels. In metastasis, on the other hand, the peritumoral region contains no infiltrating tumor cells (6,7).
Advanced MR imaging techniques are increasingly used to obtain physiologic and metabolic information that complements the anatomic images provided at conventional MR imaging. Dynamic, contrast material–enhanced perfusion-weighted MR imaging provides noninvasive physiologic measurements of tumor vascularity. Relative cerebral blood volume (rCBV) maps derived from perfusion-weighted MR can be used to identify and quantify areas of neovascularization. Perfusion MR imaging has become an important means of characterizing intracranial neoplasms (8–10). Spectroscopic MR imaging allows differentiation of tumoral versus nontumoral tissue, primarily through differences in choline metabolite, which reflects the cellular density and rate of cellular membrane turnover.
The purpose of this study was to determine whether perfusion-weighted and proton spectroscopic MR can be used to differentiate high-grade primary gliomas and solitary metastases on the basis of differences in vascularity and metabolite levels in peritumoral regions.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Among 33 patients with high-grade gliomas, there were 28 glioblastoma multiformes and five anaplastic astrocytomas. In 18 patients with metastatic tumor, two were melanomas and 16 were carcinomas, 12 from known primary (two renal, three breast, four lung, two gastric, one mucinous adenocarcinoma from colon) and four from an unknown primary site.
Imaging was performed with a 1.5-T MR unit (Siemens Vision, Iselin, NJ). Before imaging, an 18- or 20-gauge intravenous catheter was inserted in the antecubital area for contrast agent administration.
Conventional imaging.—Localizing sagittal T1-weighted images were obtained, followed by transverse T2-weighted (3,400/119 [repetition time msec/echo time msec]) and transverse fluid-attenuated inversion recovery (9,000/110; inversion time, 2,500) images. Postcontrast transverse (600/14) and sagittal T1-weighted images were obtained after perfusion-weighted and before spectroscopic MR imaging.
Perfusion-weighted MR imaging.—A series of 60 T2*-weighted gradient-echo echo-planar (1,000/54) images were obtained during the first pass of a bolus of gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ) at a dose of 0.1 mmol per kilogram of body weight. The section thickness and location of the perfusion-weighted MR dataset was determined by using the transverse T2-weighted and fluid-attenuated inversion recovery images to locate the lesion and the peritumoral T2 signal abnormality.
Spectroscopic MR imaging.—Spectroscopic data were obtained after gadopentetate dimeglumine administration. Three-dimensional selective excitation was used to excite a rectangular section, and the size of the section was dependent on the location and size of the lesion. Phase encoding was then used to generate a two-dimensional array of spectra in the section. The section was positioned to include the enhancing lesion, peritumoral region, and normal contralateral brain parenchyma as a control, while avoiding contamination from scalp fat. Other parameters were as follows: Chemical shift selective saturation, or CHESS, for water suppression, two averages; and point-resolved spectroscopy, or PRESS, selection method (1,500/135); acquisition time, 12 minutes 55 seconds. A 16 x 16 transverse phase-encoding matrix was used to obtain a two-dimensional array of spectra, with a field of view of 16 x 16. This provided spectral maps with a matrix of 8 x 8, with each voxel having a nominal voxel size of 1 x 1 x 1.5 cm, or 1 x 1 x 2 cm, depending on the thickness of the section. The term "spectroscopic MR" imaging is used synonymously with multivoxel spectroscopy, MR spectroscopic imaging, or chemical shift imaging spectroscopy. All spectroscopic MR studies were multivoxel and/or chemical shift and/or MR spectroscopic imaging acquisitions.
Data Processing
Perfusion-weighted MR imaging.—Raw perfusion-weighted MR data were processed offline as previously described by Knopp et al (9). The peritumoral signal abnormality was divided into two regions to allow investigation of whether rCBV varies with distance from the enhancing portion of the tumor. The immediate peritumoral area was defined to be within a 1-cm distance from the outer enhancing tumor margin; the distant peritumoral region was defined as greater than 1 cm from the tumor. The rCBV values were calculated in three to five regions of interest within both areas of the peritumoral region and within the enhancing tumor. Maximal rCBV (region of interest placement) measurements were obtained by identifying regions of maximal perfusion from color maps. Region of interest size was 1–5 mm in diameter (depending on the size of the lesion) and was placed by one of three authors (M.L., S.C., E.A.K.) based on the color overlap maps. Three regions of interest were placed in and around the smaller lesions, whereas the larger lesions allowed placement of up to five regions of interest.
Spectroscopic MR imaging.—Spectra were processed by using an offline workstation with standard software (Siemens). The time domain signal was apodized, processed to remove the residual water signal, Fourier transformed, baseline corrected, and phase corrected. In most cases, these processes were automatic, but where spectra appeared distorted, manual processing was used, particularly for phase correction. Gaussian filters were automatically fitted to choline, creatine, and N-acetylaspartate peaks and peak area ratios (choline-to-creatine ratio [Cho/Cr] and N-acetylaspartate–to-creatine ratio [NAA/Cr]) were calculated. Where present, lipids and lactate ratios relative to creatine were noted. Metabolite ratios were calculated in the multiple voxels; however, only the maximal values in the three locations—within the enhancing tumor, the peritumoral region, and in normal contralateral brain parenchyma—were included, and spectra with these maximal values were identified from spectral maps. Immediate and distant peritumoral spectra were not obtainable in most instances (nine of the 17 patients who underwent spectroscopic MR) because the voxel size was not small enough to allow separation between these two locations at spectroscopy; the pixel size for perfusion-weighted MR imaging allowed for differentiation between immediate and distant peritumoral regions.
The rCBV measurements were obtained from the perfusion-weighted MR data, and the Student t test was used to determine the statistical difference in rCBV between high-grade gliomas and metastases. Metabolic ratios obtained from spectroscopic MR imaging data between high-grade gliomas and metastases were also compared by using the Student t test. A P value of less than .05 indicated a statistically significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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If not amenable to chemotherapy, then modern radiation therapy provides options such as gamma knife treatment, proton beam treatment, and brachytherapy. At conventional MR imaging it is sometimes difficult to differentiate between solitary metastasis and high-grade glioma.
Most previous investigators have not found a significant difference in the intratumoral spectra of metastases and high-grade gliomas, although a small number of early study findings suggested possible spectral differences between metastases and gliomas. To our knowledge, these findings have not been reproduced (11). Bruhn et al (12) reported a series of nine primary and metastatic tumors. It was shown that there was an increase in choline in both metastases and gliomas within the enhancing tumor, and the intratumoral spectra did not allow differentiation between the two tumor types. Our study differs in that we are investigating the peritumoral rather than intratumoral spectra and rCBV.
Our study demonstrates that rCBV and Cho/Crs obtained from the peritumoral region of solitary metastasis and primary gliomas differ significantly. We believe that these findings are consistent with known pathophysiologic findings (6,7,13–15).
A pathologic examination, the capillary endothelium of metastatic tumors demonstrates increased permeability. These abnormal capillaries are similar to capillaries from the tissue of origin (15). T2-weighted areas of hyperintensity seen in peritumoral regions surrounding metastases is likely to be due to vasogenic edema associated with the leakiness of these abnormal capillaries. Furthermore, animal studies (16) of cerebral perfusion have shown that blood flow in edematous tissue is decreased due to local compression of the microcirculation by extravasated edema fluid. These two factors may account for the decrease in rCBV in the peritumoral region of metastases.
In high-grade gliomas, the enhancing portion of the tumor demonstrates breakdown of the blood-brain barrier. However, within the peritumoral region, the neural vasculature is relatively impervious (17), and the peritumoral T2 hyperintensity is at least partially due to tumor infiltration (6), possibly explaining the increased rCBV. Choline is known to be increased in the presence of tumoral tissue because of increased membrane turnover and cellular proliferation (3) and hence should be elevated in areas of tumoral infiltration, even in the absence of enhancement or T2 signal abnormality. We have demonstrated in this study that measuring the intratumoral choline is often not as useful as measuring the peritumoral choline to differentiate between high-grade gliomas and metastases.
In our study, the mean rCBV value within the peritumoral region in high-grade gliomas was 1.31 ± 0.97 (ie, more than in normal white matter), which suggests increased peritumoral perfusion due to tumor infiltration. Furthermore, the distant peritumoral region shows less perfusion and lower rCBV, consistent with diminishing tumoral infiltration.
The mean rCBV surrounding metastatic tumors was 0.39 (much lower than that of surrounding white matter), which is consistent with compression of capillaries by vasogenic edema. Furthermore, rCBV values increased as one moved from the immediate to the distant peritumoral region. Once again, this is consistent with vasogenic edema gradually decreasing to allow more perfusion farther from the tumor (16).
There was no significant difference in peritumoral NAA/Cr between the two groups because there is no neuronal replacement or destruction in the peritumoral regions of either pathologic condition. In high-grade gliomas, tumor cells infiltrate along vascular channels but do not destroy the preexisting cytoarchitecture (9). Vasogenic edema associated with metastases is also a passive process that does not necessarily destroy the underlying structure or neuronal tissue (15). There was also no appreciable difference in the tumoral NAA/Crs between the two tumor types.
Elevated Cho/Cr (2.28 ± 1.24) was found in the peritumoral regions of high-grade gliomas in keeping with tumoral infiltration. No increase in the Cho/Cr (0.76 ± 0.23) was found in the peritumoral region of metastases, which again suggests vasogenic edema. In a number of metastatic lesions, there is a diminution of metabolites in keeping with true vasogenic edema and gliosis. Interestingly, comparing the peritumoral Cho/Cr with normal white matter, the Cho/Cr values demonstrated a significant difference (P = .005) in the high-grade glioma group, whereas there was no significant difference (P = .4) in the metastatic tumor group (Table 2). Once again, this supports the fact that the peritumoral region surrounding gliomas is infiltrated and significantly different from normal white matter. Our findings are consistent with those of Burtscher et al (18), who examined 26 patients with intracranial tumors and found that gliomas and lymphomas demonstrated pathologic spectra outside the area of contrast enhancement, while four noninfiltrating tumors (meningioma, pineocytoma, germinoma, and metastasis) showed no pathologic spectra outside the region of enhancement.
From a clinical and conventional imaging point of view, once metastases are resected, the peritumoral T2 signal abnormality usually resolves completely. Hence, the region of T2 signal abnormality is purely vasogenic edema with no infiltrating metastatic tumor, unlike the T2 signal abnormality surrounding high-grade gliomas. After apparent gross total resection of a high-grade glioma, there can be recurrence within the surgical bed or unresected peritumoral T2 signal abnormality due to tumor infiltration within this region.
It has been previously reported (1–3) that metabolite ratios are similar in metastatic lesions and high-grade gliomas, and, even with multivoxel metabolic mapping techniques, spectroscopic MR imaging does not enable discrimination between a diagnosis of high-grade glioma and metastasis (4,5). We found a substantial difference in the intratumoral Cho/Cr between gliomas and metastases, 3.92 and 1.84, respectively. This may reflect the fact that the majority of the gliomas in our cohort were glioblastoma multiforme, in which extremely high levels of choline may be expected. However, as previously reported (5), because of necrosis, glioblastomas can have a lower overall Cho/Cr than can anaplastic astrocytomas. In this group of patients, the small number of anaplastic astrocytomas (n = 5) did not allow an adequate comparison of rCBV and Cho/Cr with those of glioblastomas.
The advantages of multivoxel spectroscopic imaging over single-voxel techniques in tumor imaging warrant further investigation. The utility of single-voxel spectroscopy has already been demonstrated (1–3). Sampling the entire tumor, the peritumoral region, and normal-appearing brain increases the likelihood of demonstrating the most metabolically active portion of the tumor. Only a small number of samples can be acquired by using single-voxel methods, so that one can never be certain that the most metabolically active portion of the lesion has been sampled, which is a problem faced by neuropathologists when presented with a brain biopsy specimen. It has been shown (19) that voxel position is critical when investigating lesions by using single-voxel spectroscopy. This problem is exacerbated if samples must also be acquired in peritumoral areas. Two-dimensional spectroscopic MR imaging and metabolic mapping allow simultaneous acquisition of a large volume of brain tissue in a relatively short time (4,5,20). More recently, three-dimensional spectroscopic MR imaging has been shown (21) to allow examination of the entire tumor volume.
The term peritumoral is one that warrants further discussion. In this study, it is used to describe the region of abnormal T2 signal abnormality surrounding the enhancing portion of tumor. However, as already demonstrated, the true margin of a tumor in high-grade gliomas is not defined by the region of T1 contrast enhancement; often, it is also not defined by the margin of T2 signal abnormality. The true peritumoral region is commonly found in normal-appearing brain parenchyma at conventional imaging. We are finding that advanced MR techniques such as perfusion-weighted and spectroscopic MR are now demonstrating tumoral tissue in a normal-appearing brain. Hence, the term peritumoral is perhaps not an accurate one, and the term peri-enhancing region provides a more reasonable description of the region of abnormal T2 signal surrounding gliomas.
In conclusion, spectroscopic and perfusion-weighted MR imaging are advanced MR techniques that are used to measure vastly different parameters. However, as we have shown here and as others (22,23) have shown previously, these techniques can add important physiologic and metabolic information to that obtained with conventional MR imaging. This study demonstrates that perfusion-weighted and spectroscopic MR measurements in the peritumoral region can be used to demonstrate differences in solitary metastases and high-grade gliomas.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, E.A.K., A.W.L.; study concepts and design, M.L., S.C.; literature research, M.L., J.A.; clinical studies, E.A.K.; data acquisition, M.L., J.A.; data analysis/interpretation, M.L., S.C., J.A.; statistical analysis, M.L., G.J.; manuscript preparation, M.L., S.C.; manuscript definition of intellectual content, M.L., A.L.; manuscript editing, M.L., E.A.K.; manuscript revision/review, E.A.K., S.C., G.J.; manuscript final version approval, E.A.K., G.J., A.L.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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N. Bulakbasi, M. Kocaoglu, F. Ors, C. Tayfun, and T. Ucoz Combination of Single-Voxel Proton MR Spectroscopy and Apparent Diffusion Coefficient Calculation in the Evaluation of Common Brain Tumors AJNR Am. J. Neuroradiol., February 1, 2003; 24(2): 225 - 233. [Abstract] [Full Text] [PDF]
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A. M. Saindane, S. Cha, M. Law, X. Xue, E. A. Knopp, and D. Zagzag Proton MR Spectroscopy of Tumefactive Demyelinating Lesions AJNR Am. J. Neuroradiol., September 1, 2002; 23(8): 1378 - 1386. [Abstract] [Full Text] [PDF]
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