Abstract
Several studies evaluated the predictive value of dynamic susceptibility contrast enhanced (DSC) imaging and arterial spin labeling (ASL) with regard to histological grade. Yet still less is known about their significance in terms of patients prognosis. Our purpose was to evaluate the agreement between them and the prognostic value of ASL- and DSC-CBF measurements for time-to-recurrence (TTR). Sixty nine cases of WHO Grade 3–4 gliomas underwent both DSC- and ASL-MRI. Normalized ASL and DSC-based cerebral blood flow (CBF) maps as well as DSC-derived cerebral blood volume maps (CBV) were analyzed. Wilcoxon test and Bland–Altman plot analysis were applied in order to compare DSC-rCBF and ASL-rCBF. Spearman’s rank correlation coefficients were determined for all perfusion parameters. Receiver operating characteristic (ROC) curve and survival curve analyses were performed. The median values of ASL-rCBF, DSC-rCBF, and DSC-rCBV were 5.3, 6.9, and 8.0, respectively. There was neither significant correlation nor difference between ASL-rCBF and DSC-rCBF. Slight proportional bias was demonstrated in the Bland–Altman plot analysis of ASL-rCBF and DSC-rCBF values. Unlikely to DSC-rCBV, DSC- and ASL-based rCBF parameters demonstrated moderate sensitivity and specifitity for tumor recurrence but no statistical significance regarding their prognostic values for TTR in the Kaplan–Meier analysis. There were neither correlation nor interchangeability between the DSC-rCBF and ASL-rCBF estimations, which demonstrated comparable, though not significant prognostic value for the prediction of TTR. rCBV measurements seem to provide the best sensitivity and specificity to predict tumor recurrence and survival time in these patients.
Similar content being viewed by others
References
Law M, Young R, Babb J, Rad M, Sasaki T, Zagzag D, Johnson G (2006) Comparing perfusion metrics obtained from a single compartment versus pharmacokinetic modeling methods using dynamic susceptibility contrast-enhanced perfusion MR imaging with glioma grade. AJNR Am J Neuroradiol 27(9):1975–1982
Law M, Yang S, Babb JS, Knopp EA, Golfinos JG, Zagzag D, Johnson G (2004) Comparison of cerebral blood volume and vascular permeability from dynamic susceptibility contrast-enhanced perfusion MR imaging with glioma grade. AJNR Am J Neuroradiol 25(5):746–755
Law M, Oh S, Babb JS, Wang E, Inglese M, Zagzag D, Knopp EA, Johnson G (2006) Low-grade gliomas: dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging–prediction of patient clinical response. Radiology 238(2):658–667. doi:10.1148/radiol.2382042180
Bisdas S, Kirkpatrick M, Giglio P, Welsh C, Spampinato MV, Rumboldt Z (2009) Cerebral blood volume measurements by perfusion-weighted MR imaging in gliomas: ready for prime time in predicting short-term outcome and recurrent disease? AJNR Am J Neuroradiol 30(4):681–688. doi:10.3174/ajnr.A1465
Provenzale JM, Mukundan S, Barboriak DP (2006) Diffusion-weighted and perfusion MR imaging for brain tumor characterization and assessment of treatment response1. Radiology 239(3):632–649. doi:10.1148/radiol.2393042031
Sadowski EA, Bennett LK, Chan MR, Wentland AL, Garrett AL, Garrett RW, Djamali A (2007) Nephrogenic systemic fibrosis: risk factors and incidence estimation1. Radiology 243(1):148–157. doi:10.1148/radiol.2431062144
Weber MA, Gunther M, Lichy MP, Delorme S, Bongers A, Thilmann C, Essig M, Zuna I, Schad LR, Debus J, Schlemmer HP (2003) Comparison of arterial spin-labeling techniques and dynamic susceptibility-weighted contrast-enhanced MRI in perfusion imaging of normal brain tissue. Invest Radiol 38(11):712–718. doi:10.1097/01.rli.0000084890.57197.54
Wong AM, Yan FX, Liu HL (2014) Comparison of three-dimensional pseudo-continuous arterial spin labeling perfusion imaging with gradient-echo and spin-echo dynamic susceptibility contrast MRI. J Magn Reson Imaging: JMRI 39(2):427–433. doi:10.1002/jmri.24178
Warmuth C, Gunther M, Zimmer C (2003) Quantification of blood flow in brain tumors: comparison of arterial spin labeling and dynamic susceptibility-weighted contrast-enhanced MR imaging. Radiology 228(2):523–532. doi:10.1148/radiol.2282020409
Jarnum H, Steffensen EG, Knutsson L, Frund ET, Simonsen CW, Lundbye-Christensen S, Shankaranarayanan A, Alsop DC, Jensen FT, Larsson EM (2010) Perfusion MRI of brain tumours: a comparative study of pseudo-continuous arterial spin labelling and dynamic susceptibility contrast imaging. Neuroradiology 52(4):307–317. doi:10.1007/s00234-009-0616-6
Lehmann P, Monet P, de Marco G, Saliou G, Perrin M, Stoquart-Elsankari S, Bruniau A, Vallee JN (2010) A comparative study of perfusion measurement in brain tumours at 3 Tesla MR: arterial spin labeling versus dynamic susceptibility contrast-enhanced MRI. Eur Neurol 64(1):21–26. doi:10.1159/000311520
White CM, Pope WB, Zaw T, Qiao J, Naeini KM, Lai A, Nghiemphu PL, Wang JJ, Cloughesy TF, Ellingson BM (2014) Regional and Voxel-Wise Comparisons of Blood Flow Measurements Between Dynamic Susceptibility Contrast Magnetic Resonance Imaging (DSC-MRI) and Arterial Spin Labeling (ASL) in Brain Tumors. J Neuroimaging 24(1):23–30. doi:10.1111/j.1552-6569.2012.00703.x
Wong EC, Buxton RB, Frank LR (1997) Implementation of quantitative perfusion imaging techniques for functional brain mapping using pulsed arterial spin labeling. NMR Biomed 10(4–5):237–249
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 Am J Neuroradiol 27(4):859–867
Tofts P (2005) Quantitative MRI of the brain: measuring changes caused by disease. Wiley, New York
Stecco A, Pisani C, Quarta R, Brambilla M, Masini L, Beldi D, Zizzari S, Fossaceca R, Krengli M, Carriero A (2011) DTI and PWI analysis of peri-enhancing tumoral brain tissue in patients treated for glioblastoma. J Neurooncol 102(2):261–271. doi:10.1007/s11060-010-0310-x
Buxton RB, Frank LR, Wong EC, Siewert B, Warach S, Edelman RR (1998) A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn Reson Med 40(3):383–396
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(3):797–803
Hirai T, Kitajima M, Nakamura H, Okuda T, Sasao A, Shigematsu Y, Utsunomiya D, Oda S, Uetani H, Morioka M, Yamashita Y (2011) Quantitative blood flow measurements in gliomas using arterial spin-labeling at 3T: intermodality agreement and inter- and intraobserver reproducibility study. AJNR Am J Neuroradiol 32(11):2073–2079. doi:10.3174/ajnr.A2725
Bastin ME, Carpenter TK, Armitage PA, Sinha S, Wardlaw JM, Whittle IR (2006) Effects of dexamethasone on cerebral perfusion and water diffusion in patients with high-grade glioma. AJNR Am J Neuroradiol 27(2):402–408
Chawla S, Wang S, Wolf RL, Woo JH, Wang J, O’Rourke DM, Judy KD, Grady MS, Melhem ER, Poptani H (2007) Arterial spin-labeling and MR spectroscopy in the differentiation of gliomas. AJNR Am J Neuroradiol 28(9):1683–1689. doi:10.3174/ajnr.A0673
Ludemann L, Warmuth C, Plotkin M, Forschler A, Gutberlet M, Wust P, Amthauer H (2009) Brain tumor perfusion: comparison of dynamic contrast enhanced magnetic resonance imaging using T1, T2, and T2* contrast, pulsed arterial spin labeling, and H2(15)O positron emission tomography. Eur J Radiol 70(3):465–474. doi:10.1016/j.ejrad.2008.02.012
Eichling JO, Raichle ME, Grubb RL Jr, Ter-Pogossian MM (1974) Evidence of the limitations of water as a freely diffusible tracer in brain of the rhesus monkey. Circ Res 35(3):358–364
St Lawrence KS, Frank JA, McLaughlin AC (2000) Effect of restricted water exchange on cerebral blood flow values calculated with arterial spin tagging: a theoretical investigation. Magn Reson Med 44(3):440–449
Sakaie KE, Shin W, Curtin KR, McCarthy RM, Cashen TA, Carroll TJ (2005) Method for improving the accuracy of quantitative cerebral perfusion imaging. J Magn Reson imaging 21(5):512–519. doi:10.1002/jmri.20305
Lu H, Clingman C, Golay X, van Zijl PC (2004) Determining the longitudinal relaxation time (T1) of blood at 3.0 Tesla. Magn Reson Med 52(3):679–682. doi:10.1002/mrm.20178
Koziak AM, Winter J, Lee TY, Thompson RT, St Lawrence KS (2008) Validation study of a pulsed arterial spin labeling technique by comparison to perfusion computed tomography. Magn Reson Imaging 26(4):543–553. doi:10.1016/j.mri.2007.10.005
Furtner J, Schopf V, Schewzow K, Kasprian G, Weber M, Woitek R, Asenbaum U, Preusser M, Marosi C, Hainfellner JA, Widhalm G, Wolfsberger S, Prayer D (2014) Arterial spin-labeling assessment of normalized vascular intratumoral signal intensity as a predictor of histologic grade of astrocytic neoplasms. AJNR Am J Neuroradiol 35(3):482–489. doi:10.3174/ajnr.A3705
Boxerman JL, Hamberg LM, Rosen BR, Weisskoff RM (1995) MR contrast due to intravascular magnetic susceptibility perturbations. Magn Reson Med 34(4):555–566
Kennan RP, Zhong J, Gore JC (1994) Intravascular susceptibility contrast mechanisms in tissues. Magn Reson Med 31(1):9–21
Petersen ET, Zimine I, Ho YC, Golay X (2006) Non-invasive measurement of perfusion: a critical review of arterial spin labelling techniques. Br J Radiol 79(944):688–701. doi:10.1259/bjr/67705974
Kety SS (1951) The theory and applications of the exchange of inert gas at the lungs and tissues. Pharmacol Rev 3(1):1–41
Hirai T, Murakami R, Nakamura H, Kitajima M, Fukuoka H, Sasao A, Akter M, Hayashida Y, Toya R, Oya N, Awai K, Iyama K, Kuratsu JI, Yamashita Y (2008) Prognostic value of perfusion MR imaging of high-grade astrocytomas: long-term follow-up study. AJNR Am J Neuroradiol 29(8):1505–1510. doi:10.3174/ajnr.A1121
Lev MH, Ozsunar Y, Henson JW, Rasheed AA, Barest GD, Harsh GRT, Fitzek MM, Chiocca EA, Rabinov JD, Csavoy AN, Rosen BR, Hochberg FH, Schaefer PW, Gonzalez RG (2004) Glial tumor grading and outcome prediction using dynamic spin-echo MR susceptibility mapping compared with conventional contrast-enhanced MR: confounding effect of elevated rCBV of oligodendrogliomas [corrected]. AJNR Am J Neuroradiol 25(2):214–221
Law M, Oh S, Johnson G, Babb JS, Zagzag D, Golfinos J, Kelly PJ (2006) Perfusion magnetic resonance imaging predicts patient outcome as an adjunct to histopathology: a second reference standard in the surgical and nonsurgical treatment of low-grade gliomas. Neurosurgery 58(6):1099–1107. doi:10.1227/01.neu.0000215944.81730.18 discussion: 1099–1107
Mills SJ, Patankar TA, Haroon HA, Baleriaux D, Swindell R, Jackson A (2006) Do cerebral blood volume and contrast transfer coefficient predict prognosis in human glioma? AJNR Am J Neuroradiol 27(4):853–858
Noguchi T, Yoshiura T, Hiwatashi A, Togao O, Yamashita K, Nagao E, Shono T, Mizoguchi M, Nagata S, Sasaki T, Suzuki SO, Iwaki T, Kobayashi K, Mihara F, Honda H (2008) Perfusion imaging of brain tumors using arterial spin-labeling: correlation with histopathologic vascular density. AJNR Am J Neuroradiol 29(4):688–693. doi:10.3174/ajnr.A0903
Miyagami M, Katayama Y (2005) Angiogenesis of glioma: evaluation of ultrastructural characteristics of microvessels and tubular bodies (Weibel-Palade) in endothelial cells and immunohistochemical findings with VEGF and p53 protein. Med Mol Morphol 38(1):36–42. doi:10.1007/s00795-004-0273-0
Ostergaard L, Hochberg FH, Rabinov JD, Sorensen AG, Lev M, Kim L, Weisskoff RM, Gonzalez RG, Gyldensted C, Rosen BR (1999) Early changes measured by magnetic resonance imaging in cerebral blood flow, blood volume, and blood-brain barrier permeability following dexamethasone treatment in patients with brain tumors. J Neurosurg 90(2):300–305. doi:10.3171/jns.1999.90.2.0300
Wilkinson ID, Jellineck DA, Levy D, Giesel FL, Romanowski CA, Miller BA, Griffiths PD (2006) Dexamethasone and enhancing solitary cerebral mass lesions: alterations in perfusion and blood-tumor barrier kinetics shown by magnetic resonance imaging. Neurosurgery 58(4):640–646. doi:10.1227/01.NEU.0000204873.68395.A0 discussion 640–646
Alsop DC, Detre JA, Golay X, Gunther M, Hendrikse J, Hernandez-Garcia L, Lu H, Macintosh BJ, Parkes LM, Smits M, van Osch MJ, Wang DJ, Wong EC, Zaharchuk G (2014) Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med. doi:10.1002/mrm.25197
Macintosh BJ, Marquardt L, Schulz UG, Jezzard P, Rothwell PM (2012) Hemodynamic alterations in vertebrobasilar large artery disease assessed by arterial spin-labeling MR imaging. AJNR Am J Neuroradiol 33(10):1939–1944. doi:10.3174/ajnr.A3090
Furtner J, Bender B, Braun C, Schittenhelm J, Skardelly M, Ernemann U, Bisdas S (2014) Prognostic value of blood flow measurements using arterial spin labeling in gliomas. PLoS ONE 9(6):e99616. doi:10.1371/journal.pone.0099616
MacIntosh BJ, Filippini N, Chappell MA, Woolrich MW, Mackay CE, Jezzard P (2010) Assessment of arterial arrival times derived from multiple inversion time pulsed arterial spin labeling MRI. Magn Reson Med 63(3):641–647. doi:10.1002/mrm.22256
van Westen D, Petersen ET, Wirestam R, Siemund R, Bloch KM, Stahlberg F, Bjorkman-Burtscher IM, Knutsson L (2011) Correlation between arterial blood volume obtained by arterial spin labelling and cerebral blood volume in intracranial tumours. Magma 24(4):211–223. doi:10.1007/s10334-011-0255-x
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rau, M.K., Braun, C., Skardelly, M. et al. Prognostic value of blood flow estimated by arterial spin labeling and dynamic susceptibility contrast-enhanced MR imaging in high-grade gliomas. J Neurooncol 120, 557–566 (2014). https://doi.org/10.1007/s11060-014-1586-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11060-014-1586-z