Abstract
Purpose
Increased relative cerebral blood volume (rCBV) was previously found in peritumoural oedema of glioblastomas (GBM). Supposing that peritumoural rCBV is not increased in metastases, we aimed to evaluate whether rCBV values of the whole peritumoural area are accurate to differentiate solitary metastasis from GBM irrespective of the peritumoural oedema.
Methods
Contrast-enhanced T1-weighted (T1-w) and T2*-weighted dynamic susceptibility contrast MRI was performed in 52 patients with contrast-enhancing solitary brain tumours before surgery. In each T1-w slice depicting the contrast-enhancing tumour, a rim within approximately 15 mm was defined in the peritumoural area. The rCBV values were normalised to rCBV values of the contralateral normal white matter. Differences between metastases and GBM for normalised rCBV values for each slice were determined with the Mann–Whitney U test (p < 0.05).
Results
Histopathological examination revealed 29 GBM and 23 metastases. Peritumoural rCBV was significantly lower in metastases than in GBM (p < 0.01). Using the cutoff value 1.0 for discriminating metastases from GBM yielded a sensitivity of 96%, specificity of 64%, a positive predictive value of 68% and a negative predictive value of 95%.
Conclusions
The rCBV in the peritumoural area of contrast-enhancing brain tumours has a high diagnostic accuracy to discriminate metastases from GBM irrespective of surrounding oedema and without the bias of slice selection and ROI positioning. Metastases should be excluded, if at least one tumour-depicting slice reveals an increase of peritumoural rCBV compared to the normal contralateral brain (normalised rCBV value >1). Conversely, the decrease of peritumoural rCBV may not reliably exclude GBM.
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References
Aronen HJ, Gazit IE, Louis DN, Buchbinder BR, Pardo FS, Weisskoff RM, Harsh GR, Cosgrove GR, Halpern EF, Hochberg FH et al (1994) Cerebral blood volume maps of gliomas: comparison with tumor grade and histologic findings. Radiology 191:41–51
Aronen HJ, Perkio J (2002) Dynamic susceptibility contrast MRI of gliomas. Neuroimaging Clin N Am 12:501–523
Blasel S, Franz K, Mittelbronn M, Morawe G, Jurcoane A, Pellikan S, Zanella F, Hattingen E (2010) The striate sign: peritumoral perfusion pattern of infiltrative primary and recurrence gliomas. Neurosurgical Rev 33:193–204
Boxerman JL, Schmainda KM, Weisskoff RM (2006) Relative cerebral blood volume maps corrected for contrast agent extravasation significantly correlate with glioma tumor grade, whereas uncorrected maps do not. AJNR 27:859–867
Bulakbasi N, Kocaoglu M, Farzaliyev A, Tayfun C, Ucoz T, Somuncu I (2005) Assessment of diagnostic accuracy of perfusion MR imaging in primary and metastatic solitary malignant brain tumors. AJNR 26:2187–2199
Campos S, Davey P, Hird A, Pressnail B, Bilbao J, Aviv RI, Symons S, Pirouzmand F, Sinclair E, Culleton S, Desa E, Goh P, Chow E (2009) Brain metastasis from an unknown primary, or primary brain tumour? A diagnostic dilemma. Curr Oncol 16:62–66
Cha S (2006) Update on brain tumor imaging: from anatomy to physiology. AJNR 27:475–487
Cha S, Knopp EA, Johnson G, Wetzel SG, Litt AW, Zagzag D (2002) Intracranial mass lesions: dynamic contrast-enhanced susceptibility-weighted echo-planar perfusion MR imaging. Radiology 223:11–29
Chiang IC, Kuo YT, Lu CY, Yeung KW, Lin WC, Sheu FO, Liu GC (2004) Distinction between high-grade gliomas and solitary metastases using peritumoral 3-T magnetic resonance spectroscopy, diffusion, and perfusion imagings. Neuroradiology 46:619–627
Claes A, Idema AJ, Wesseling P (2007) Diffuse glioma growth: a guerilla war. Acta Neuropathol 114:443–458
Fan G, Sun B, Wu Z, Guo Q, Guo Y (2004) In vivo single-voxel proton MR spectroscopy in the differentiation of high-grade gliomas and solitary metastases. Clin Radiol 59:77–85
Hakyemez B, Erdogan C, Gokalp G, Dusak A, Parlak M (2010) Solitary metastases and high-grade gliomas: radiological differentiation by morphometric analysis and perfusion-weighted MRI. Clin Radiol 65:15–20
Hossman KA, Bloink M (1981) Blood flow and regulation of blood flow in experimental peritumoral edema. Stroke 12:211–217
Hwang TL, Close TP, Grego JM, Brannon WL, Gonzales F (1996) Predilection of brain metastasis in gray and white matter junction and vascular border zones. Cancer 77:1551–1555
Kelly PJ, Daumas-Duport C, Scheithauer BW, Kall BA, Kispert DB (1987) Stereotactic histologic correlations of computed tomography- and magnetic resonance imaging-defined abnormalities in patients with glial neoplasms. Mayo Clin Proc 62:450–459
Knopp EA, Cha S, Johnson G, Mazumdar A, Golfinos JG, Zagzag D, Miller DC, Kelly PJ, Kricheff II (1999) Glial neoplasms: dynamic contrast-enhanced T2*-weighted MR imaging. Radiology 211:791–798
Law M, Cha S, Knopp EA, Johnson G, Arnett J, Litt AW (2002) High-grade gliomas and solitary metastases: differentiation by using perfusion and proton spectroscopic MR imaging. Radiology 222:715–721
Law M, Yang S, Wang H, Babb JS, Johnson G, Cha S, Knopp EA, Zagzag D (2003) Glioma grading: sensitivity, specificity, and predictive values of perfusion MR imaging and proton MR spectroscopic imaging compared with conventional MR imaging. AJNR 24:1989–1998
Lev MH, Rosen BR (1999) Clinical applications of intracranial perfusion MR imaging. Neuroimaging Clin N Am 9:309–331
Lu S, Ahn D, Johnson G, Cha S (2003) Peritumoral diffusion tensor imaging of high-grade gliomas and metastatic brain tumors. AJNR 24:937–941
Lu S, Ahn D, Johnson G, Law M, Zagzag D, Grossman RI (2004) Diffusion-tensor MR imaging of intracranial neoplasia and associated peritumoral edema: introduction of the tumor infiltration index. Radiology 232:221–228
Morita K, Matsuzawa H, Fujii Y, Tanaka R, Kwee IL, Nakada T (2005) Diffusion tensor analysis of peritumoral edema using lambda chart analysis indicative of the heterogeneity of the microstructure within edema. J Neurosurg 102:336–341
Oh J, Cha S, Aiken AH, Han ET, Crane JC, Stainsby JA, Wright GA, Dillon WP, Nelson SJ (2005) Quantitative apparent diffusion coefficients and T2 relaxation times in characterizing contrast enhancing brain tumors and regions of peritumoral edema. J Magn Reson Imaging 21:701–708
Ostergaard L, Weisskoff RM, Chesler DA, Gyldensted C, Rosen BR (1996) High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: mathematical approach and statistical analysis. Magn Reson Med 36:715–725
Posner JB (1992) Management of brain metastases. Rev Neurol (Paris) 148:477–487
Preul C, Kuhn B, Lang EW, Mehdorn HM, Heller M, Link J (2003) Differentiation of cerebral tumors using multi-section echo planar MR perfusion imaging. Eur J Radiol 48:244–251
Principi M, Italiani M, Guiducci A, Aprile I, Muti M, Giulianelli G, Ottaviano P (2003) Perfusion MRI in the evaluation of the relationship between tumour growth, necrosis and angiogenesis in glioblastomas and grade 1 meningiomas. Neuroradiology 45:205–211
Provenzale JM, Mukundan S, Barboriak DP (2006) Diffusion-weighted and perfusion MR imaging for brain tumor characterization and assessment of treatment response. Radiology 239:632–649
Rosen BR, Belliveau JW, Vevea JM, Brady TJ (1990) Perfusion imaging with NMR contrast agents. Magn Reson Med 14:249–265
Schiff D (2001) Single brain metastasis. Curr Treat Options Neurol 3:89–99
Schmainda KM, Rand SD, Joseph AM, Lund R, Ward BD, Pathak AP, Ulmer JL, Badruddoja MA, Krouwer HG (2004) Characterization of a first-pass gradient-echo spin-echo method to predict brain tumor grade and angiogenesis. AJNR 25:1524–1532
Server A, Josefsen R, Kulle B, Maehlen J, Schellhorn T, Gadmar O, Kumar T, Haakonsen M, Langberg CW, Nakstad PH (2010) Proton magnetic resonance spectroscopy in the distinction of high-grade cerebral gliomas from single metastatic brain tumors. Acta Radiol 51:316–325
Sugahara T, Korogi Y, Kochi M, Ikushima I, Hirai T, Okuda T, Shigematsu Y, Liang L, Ge Y, Ushio Y, Takahashi M (1998) Correlation of MR imaging-determined cerebral blood volume maps with histologic and angiographic determination of vascularity of gliomas. AJR 171:1479–1486
Uematsu H, Maeda M (2006) Double-echo perfusion-weighted MR imaging: basic concepts and application in brain tumors for the assessment of tumor blood volume and vascular permeability. Eur Radiol 16:180–186
Wang S, Kim S, Chawla S, Wolf RL, Zhang WG, O’Rourke DM, Judy KD, Melhem ER, Poptani H (2009) Differentiation between glioblastomas and solitary brain metastases using diffusion tensor imaging. Neuroimage 44:653–660
Wetzel SG, Cha S, Johnson G, Lee P, Law M, Kasow DL, Pierce SD, Xue X (2002) Relative cerebral blood volume measurements in intracranial mass lesions: interobserver and intraobserver reproducibility study. Radiology 224:797–803
Young GS, Setayesh K (2009) Spin-echo echo-planar perfusion MR imaging in the differential diagnosis of solitary enhancing brain lesions: distinguishing solitary metastases from primary glioma. AJNR 30:575–577
Zhang M, Olsson Y (1997) Hematogenous metastases of the human brain-characteristics of peritumoral brain changes: a review. J Neurooncol 35:81–89
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The purpose of this investigation was to analyse the challenging issue of the preoperative discrimination between solitary metastasis and glioblastoma. The authors evaluated rCBV values of the peritumoural area that they considered as the 15-mm-wide rim outside the outer contrast-enhancing tumour. One element of originality in this study consists of measuring the rCBV of the entire peritumoural area without the bias of ROI selection as reported by previous investigations. In the presented study, rCBV values were significantly lower in metastases than in GBM and a cutoff value was finally proposed to differentiate metastases from GBM. The technique is able to discriminate metastases from GBMs with a sensitivity of 96% and a specificity of 64%. We believe that it may provide additional useful data in the current neuro-oncological setting.
Domenico d’Avella
Alessandro Della Puppa
Padua, Italy
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Blasel, S., Jurcoane, A., Franz, K. et al. Elevated peritumoural rCBV values as a mean to differentiate metastases from high-grade gliomas. Acta Neurochir 152, 1893–1899 (2010). https://doi.org/10.1007/s00701-010-0774-7
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DOI: https://doi.org/10.1007/s00701-010-0774-7