Contrast-enhanced magnetic resonance imaging of central nervous system tumors: Agents, mechanisms, and applications

Topics in Magnetic Resonance Imaging

Volumn 17, Issue 2, 2006, Pages 89-106

  Essig, Marco ^a   Weber, Marc André ^a   Von Tengg Kobligk, Hendrik ^a   Knopp, Michael V ^b   Yuh, William T C ^b   Giesel, Frederik L ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Brain tumors; Contrast media; DCE MRI; DSC MRI; MRI

Indexed keywords

CONTRAST MEDIUM; FERUCARBOTRAN; GADOBENATE DIMEGLUMINE; GADOBUTROL; GADODIAMIDE; GADOFOSVESET; GADOLINIUM PENTETATE; GADOLINIUM PENTETATE MEGLUMINE; GADOTERATE MEGLUMINE; GADOTERIDOL; GADOVERSETAMIDE; GADOXETIC ACID; MANGAFODIPIR; SUPERPARAMAGNETIC IRON OXIDE; UNCLASSIFIED DRUG;

CENTRAL NERVOUS SYSTEM TUMOR; CONTRAST ENHANCEMENT; DRUG PROTEIN BINDING; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REVIEW;

CENTRAL NERVOUS SYSTEM NEOPLASMS; CONTRAST MEDIA; GADOLINIUM; HUMANS; MAGNETIC RESONANCE IMAGING; ORGANOMETALLIC COMPOUNDS; RADIOGRAPHIC IMAGE ENHANCEMENT;

EID: 33845991496     PISSN: 08993459     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.rmr.0000245464.36148.dc     Document Type: Review

References (116)

1. Ohgaki H, Kleihues P. Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol. 2005;64(6):479-489.
2. Cenacchi G, Giangaspero F. Emerging tumor entities and variants of CNS neoplasms. J Neuropathol Exp Neurol. 2004;63(3):185-192.
3. Behin A, Hoang-Xuan K, Carpentier AF, et al. Primary brain tumours in adults. Lancet. 2003;361(9354):323-331.
4. Stieber VW. Low-grade gliomas. Curr Treat Options Oncol. 2001;2(6):495-506.
5. Ohgaki H, Kleihues P. Epidemiology and etiology of gliomas. Acta Neuropathol. 2005;109:93-108.
6. Walker AE, Robins M, Weinfeld FD. Epidemiology of brain tumors: the national survey of intracranial neoplasms. Neurology. 1985;35(2):219-226.
7. Longstreth WT Jr, Dennis LK, McGuire VM, et al. Epidemiology of intracranial meningioma. Cancer. 1993;72(3):639-648.
8. Patchell RA. Brain metastases. Neurol Clin. 1991;9(4):817-824.
9. Brant-Zawadzki M, Norman D, Newton TH, et al. Magnetic resonance of the brain: the optimal screening technique. Radiology. 1984;152(1):71-77.
10. Muroff LR, Runge VM. The use of MR contrast in neoplastic disease of the brain. Top Magn Reson Imaging. 1995;7(3):137-157.
11. Erickson BJ, Campeau NG, Schreiner SA, et al. Triple-dose contrast/magnetization transfer suppressed imaging of "non-enhancing" brain gliomas. J Neurooncol. 2002;60(1):25-29.
12. Schneider G, Kirchin MA, Pirovano G, et al. Gadobenate dimeglumine-enhanced magnetic resonance imaging of intracranial metastases: effect of dose on lesion detection and delineation. J Magn Reson Imaging. 2001;14(5):525-539.
13. Bart J, Groen HJ, Hendrikse NH, et al. The blood-brain barrier and oncology: new insights into function and modulation. Cancer Treat Rev. 2000;26(6):449-462.
14. Neuwelt EA. Mechanisms of disease: the blood-brain barrier. Neurosurgery. 2004;54(1):131-140.
15. Gururangan S, Friedman HS. Innovations in design and delivery of chemotherapy for brain tumors. Neuroimaging Clin N Am. 2002;12(4):583-597.
16. Demeule M, Regina A, Jodoin J, et al. Drug transport to the brain: key roles for the efflux pump P-glycoprotein in the blood-brain barrier. Vascul Pharmacol. 2002;38(6):339-348.
17. Kemper EM, Boogerd W, Thuis I, et al. Modulation of the blood-brain barrier in oncology: therapeutic opportunities for the treatment of brain tumours? Cancer Treat Rev. 2004;30(5):415-423.
18. Rautioa J, Chikhale PJ. Drug delivery systems for brain tumor therapy. Curr Pharm Des. 2004;10(12):1341-1353.
19. Kroll RA, Neuwelt EA. Outwitting the blood-brain barrier for therapeutic purposes: osmotic opening and other means. Neurosurgery. 1998;42(5):1083-1099.
20. Kido G, Wright JL, Merchant RE. Acute effects of human recombinant tumor necrosis factor-alpha on the cerebral vasculature of the rat in both normal brain and in an experimental glioma model. J Neurooncol. 1991;10(2):95-109.
21. Schneider SW, Ludwig T, Tatenhorst L, et al. Glioblastoma cells release factors that disrupt blood-brain barrier features. Acta Neuropathol (Berl). 2004;107(3):272-276.
22. Earnest F, Kelly PJ, Scheithauer BW, et al. Cerebral astrocytomas: histopathologic correlation of MR and CT contrast enhancement with stereotactic biopsy. Radiology. 1988;166(3):823-827.
23. van den Bent MJ. Management of metastatic (parenchymal, leptomeningeal, and epidural) lesions. Curr Opin Oncol. 2004;16(4):309-313.
24. Fidler IJ, Yano S, Zhang RD, et al. The seed and soil hypothesis: vascularisation and brain metastases. Lancet Oncol. 2002;3(1):53-57.
25. Groothuis DR. The blood-brain and blood-tumor barriers: a review of strategies for increasing drug delivery. Neuro-oncology. 2000;2(1):45-59.
26. Holodny AI, Nusbaum AO, Festa S, et al. Correlation between the degree of contrast enhancement and the volume of peritumoral edema in meningiomas and malignant gliomas. Neuroradiology. 1999;41(11):820-825.
27. Pronin IN, Holodny AI, Petraikin AV. MRI of high-grade glial tumors: correlation between the degree of contrast enhancement and the volume of surrounding edema. Neuroradiology. 1997;39(5):348-350.
28. Runge VM. A review of contrast media research in 1999-2000. Invest Radiol. 2001;36(2):123-130.
29. Wilkinson ID, Jellineck DA, Levy D, et al. Dexamethasone and enhancing solitary cerebral mass lesions: alterations in perfusion and blood-tumor barrier kinetics shown by magnetic resonance imaging. Neurosurgery. 2006;58(4):640-646.
30. Claussen C, Laniado M, Schorner W, et al. Gadolinium-DTPA in MR imaging of glioblastomas and intracranial metastases. AJNR Am J Neuroradiol. 1985;6(5):669-674.
31. Koenig SH. From the relaxivity of Gd(DTPA)2 - to everything else. Magn Reson Med. 1991;22(2):183-190.
32. Wolf GL, Halavaara JT. Basic principles of MR contrast agents. Magn Reson Imaging Clin N Am. 1996;4(1):1-10.
33. Knopp MV, Weiss E, Sinn HP, et al. Pathophysiologic basis of contrast enhancement in breast tumors. J Magn Reson Imaging. 1999;10(3):260-266.
34. Grossman RI, Rubin DL, Hunter G, et al. Magnetic resonance imaging in patients with central nervous system pathology: a comparison of OptiMARK (Gd-DTPA-BMEA) and Magnevist (Gd-DTPA). Invest Radiol. 2000;35(7):412-419.
35. Provenzale JM, Mukundan S, Dewhirst M. The role of blood-brain barrier permeability in brain tumor imaging and therapeutics. AJR Am J Roentgenol. 2005;185(3):763-767.
36. Tirkkonen B, Aukrust A, Couture E, et al. Physicochemical characterisation of mangafodipir trisodium. Acta Radiol. 1997;38(4 Pt 2):780-789.
37. Lin YJ, Koretsky AP. Manganese ion enhances T1-weighted MRI during brain activation: an approach to direct imaging of brain function. Magn Reson Med. 1997;38(3):378-388.
38. Stieltjes B, Klussmann S, Bock M, et al. Manganese-enhanced magnetic resonance imaging for in vivo assessment of damage and functional improvement following spinal cord injury in mice. Magn Reson Med. 2006;55(5):1124-1131.
39. Huppertz A, Rohrer M. Gadobutrol, a highly concentrated MR-imaging contrast agent: its physicochemical characteristics and the basis for its use in contrast-enhanced MR angiography and perfusion imaging. Eur Radiol. 2004;14 (suppl 5):M12-M18.
40. Rohrer M, Bauer H, Mintorovitch J, et al. Comparison of magnetic properties of MRI contrast media solutions at different magnetic field strengths. Invest Radiol. 2005;40(11):715-724.
41. Tombach B, Benner T, Reimer P, et al. Do highly concentrated gadolinium chelates improve MR brain perfusion imaging? Intraindividually controlled randomized crossover concentration comparison study of 0.5 versus 1.0 mol/L gadobutrol. Radiology. 2003;226(3):880-888.
42. Essig M, Lodemann KP, Le-Huu M, et al. Intraindividual comparison of gadobenate dimeglumine and gadobutrol for cerebral magnetic resonance perfusion imaging at 1.5 T. Invest Radiol. 2006;41(3):256-263.
43. Cotton F. Diffusion-perfusion in intra-axial brain tumors with high relaxivity contrast agents. Neuroradiology. 2006;48 (suppl 1):34-40.
44. Knopp MV, Runge VM, Essig M, et al. Primary and secondary brain tumors at MR imaging: bicentric intraindividual crossover comparison of gadobenate dimeglumine and gadopentetate dimeglumine. Radiology. 2004;230(1):55-64.
45. Cavagna FM, Dapra M, Maggioni F, et al. Gd-BOPTA/Dimeg: experimental disease imaging. Magn Reson Med. 1991;22(2):329-333.
46. Grazioli L, Morana G, Kirchin MA, et al. Accurate differentiation of focal nodular hyperplasia from hepatic adenoma at gadobenate dimeglumine-enhanced MR imaging: prospective study. Radiology. 2005;236(1):166-177.
47. Helmberger T, Semelka RC. New contrast agents for imaging the liver. Magn Reson Imaging Clin N Am. 2001;9(4):745-766. [vi].
48. Schneider G, Reimer P, Mamann A, et al. Contrast agents in abdominal imaging: current and future directions. Top Magn Reson Imaging. 2005;16(1):107-124.
49. Goyen M, Debatin JF. Gadobenate dimeglumine (MultiHance) for magnetic resonance angiography: review of the literature. Eur Radiol. 2003;13 (suppl 3):N19-N27.
50. Knopp MV, Schoenberg SO, Rehm C, et al. Assessment of gadobenate dimeglumine for magnetic resonance angiography: phase I studies. Invest Radiol. 2002;37(12):706-715.
51. Kirchin MA, Pirovano GP, Spinazzi A. Gadobenate dimeglumine (Gd-BOPTA). An overview. Invest Radiol. 1998;33(11):798-809.
52. Giesel FL, Tengg-Kobligk H, Wilkinson ID, et al. Influence of human serum albumin on longitudinal and transverse relaxation rates (r1 and r2) of magnetic resonance contrast agents. Invest Radiol. 2006;41(3):222-228.
53. Vander EL, Chapelle F, Laurent S, et al. Stereospecific binding of MRI contrast agents to human serum albumin: the case of Gd-(S)-EOB-DTPA (Eovist) and its (R) isomer. J Biol Inorg Chem. 2001;6(2):196-200.
54. Saito K, Kotake F, Ito N, et al. Gd-EOB-DTPA enhanced MRI for hepatocellular carcinoma: quantitative evaluation of tumor enhancement in hepatobiliary phase. Magn Reson Med Sci. 2005;4(1):1-9.
55. Huppertz A, Haraida S, Kraus A, et al. Enhancement of focal liver lesions at gadoxetic acid-enhanced MR imaging: correlation with histopathologic findings and spiral CT - initial observations. Radiology. 2005;234(2):468-478.
56. Lauffer RB. Targeted relaxation enhancement agents for MRI. Magn Reson Med. 1991;22(2):339-342.
57. Eldredge HB, Spiller M, Chasse JM, et al. Species dependence on plasma protein binding and relaxivity of the gadolinium-based MRI contrast agent MS-325. Invest Radiol. 2006;41(3):229-243.
58. Caravan P, Cloutier NJ, Greenfield MT, et al. The interaction of MS-325 with human serum albumin and its effect on proton relaxation rates. J Am Chem Soc. 2002;124(12):3152-3162.
59. Goyen M, Shamsi K, Schoenberg SO. Vasovist-enhanced MR angiography. Eur Radiol. 2006;16 (suppl 2):B9-B14.
60. Cavagna FM, Anelli PL, Lorusso V, et al. B-22956, a new intravascular contrast agent for MR coronary angiography results. Proc Int Soc Magn Reson Med Sci. 2001:9.
61. Lorusso V, Pascolo L, Fernetti C, et al. In vitro and in vivo hepatic transport of the magnetic resonance imaging contrast agent B22956/1: role of MRP proteins. Biochem Biophys Res Commun. 2002;293(1):100-105.
62. de HC, Anelli PL, Lorusso V, et al. Gadocoletic acid trisodium salt (b22956/1): a new blood pool magnetic resonance contrast agent with application in coronary angiography. Invest Radiol. 2006;41(3):279-291.
63. La NA, Stoelben S, Scheffler K, et al. B22956/1, a new intravascular contrast agent for MRI: first administration to humans - preliminary results. Acad Radiol. 2002;9(suppl 2):S404-S406.
64. Bonnemain B. Superparamagnetic agents in magnetic resonance imaging: physicochemical characteristics and clinical applications. A review. J Drug Target. 1998;6(3):167-174.
65. Hemmingsson A, Carlsten J, Ericsson A, et al. Relaxation enhancement of the dog liver and spleen by biodegradable superparamagnetic particles in proton magnetic resonance imaging. Acta Radiol. 1987;28(6):703-705.
66. Saini S, Stark DD, Hahn PF, et al. Ferrite particles: a superparamagnetic MR contrast agent for the reticuloendothelial system. Radiology. 1987;162(1 Pt 1):211-216.
67. Reimer P, Tombach B. Hepatic MRI with SPIO: detection and characterization of focal liver lesions. Eur Radiol. 1998;8(7):1198-1204.
68. Hunt MA, Bago AG, Neuwelt EA. Single-dose contrast agent for intraoperative MR imaging of intrinsic brain tumors by using ferumoxtran-10. AJNR Am J Neuroradiol. 2005;26(5):1084-1088.
69. Taschner CA, Wetzel SG, Tolnay M, et al. Characteristics of ultrasmall superparamagnetic iron oxides in patients with brain tumors. AJR Am J Roentgenol. 2005;185(6):1477-1486.
70. Tombach B, Reimer P, Bremer C, et al. First-pass and equilibrium-MRA of the aortoiliac region with a superparamagnetic iron oxide blood pool MR contrast agent (SH U 555 C): results of a human pilot study. NMR Biomed. 2004;17(7):500-506.
71. Kellar KE, Fujii DK, Gunther W, et al. NC100150 injection, a preparation of optimized iron oxide nanoparticles for positive-contrast MR angiography. JMRI. 2000;11(5):488-494.
72. Schnorr J, Wagner S, Abramjuk C, et al. Comparison of the iron oxide-based blood-pool contrast medium VSOP-C184 with gadopentetate dimeglumine for first-pass magnetic resonance angiography of the aorta and renal arteries in pigs. Invest Radiol. 2004;39(9):546-553.
73. Verhoye M, van der Sanden BP, Rijken PF, et al. Assessment of the neovascular permeability in glioma xenografts by dynamic T[1] MRI with Gadomer-17. Magn Reson Med. 2002;47(2):305-313.
74. Corot C, Robert P, Lancelot E, et al. Distribution of gadomelitol in a human breast tumor model in mice. MAGMA. 2005;18(3):138-143.
75. Kobayashi H, Brechbiel MW. Nano-sized MRI contrast agents with dendrimer cores. Adv Drug Deliv Rev. 2005;57(15):2271-2286.
76. Anderson SA, Lee KK, Frank JA. Gadolinium-fullerenol as a paramagnetic contrast agent for cellular imaging. Invest Radiol. 2006;41(3):332-338.
77. Giesel FL, Stroick M, Griebe M, et al. Agent free mediated Gadofluorine M uptake in stem cells as a new tracking method at 1.5T MRI: an in vitro and in vivo study. Invest Radiol. In press.
78. Knopp MV, Balzer T, Esser M, et al. Assessment of utilization and pharmacovigilance based on spontaneous adverse event reporting of gadopentetate dimeglumine as a magnetic resonance contrast agent after 45 million administrations and 15 years of clinical use. Invest Radiol. 2006;41(6):491-499.
79. Yuh WT, Nguyen HD, Tali ET, et al. Delineation of gliomas with various doses of MR contrast material. AJNR Am J Neuroradiol. 1994;15(5):983-989.
80. Yuh WT, Tali ET, Nguyen HD, et al. The effect of contrast dose, imaging time, and lesion size in the MR detection of intracerebral metastasis. AJNR Am J Neuroradiol. 1995;16(2):373-380.
81. Yuh WT, Tali ET, Nguyen HD, et al. The effect of contrast dose, imaging time, and lesion size in the MR detection of intracerebral metastasis. AJNR Am J Neuroradiol. 1995;16(2):373-380.
82. Sze G, Johnson C, Kawamura Y, et al. Comparison of single- and triple-dose contrast material in the MR screening of brain metastases. AJNR Am J Neuroradiol. 1998;19(5):821-828.
83. Van DP, Sijens PE, Schmitz PI, et al. Gd-enhanced MR imaging of brain metastases: contrast as a function of dose and lesion size. Magn Reson Imaging. 1997;15(5):535-541.
84. Ba-Ssalamah A, Nobauer-Huhmann IM, Pinker K, et al. Effect of contrast dose and field strength in the magnetic resonance detection of brain metastases. Invest Radiol. 2003;38(7):415-422.
85. Haustein J, Laniado M, Niendorf HP, et al. Administration of gadopentetate dimeglumine in MR imaging of intracranial tumors: dosage and field strength. AJNR Am J Neuroradiol. 1992;13(4):1199-1206.
86. Schubeus P, Schorner W, Haustein J, et al. Optimization of gadolinium-DTPA dose: an inter-individual study of patients with intracranial tumors. RoFo. 1990;153(1):29-35.
87. Yang M, Christoforidis GA, Figueredo T, et al. Dosage determination of ultrasmall particles of iron oxide for the delineation of microvasculature in the Wistar rat brain. Invest Radiol. 2005;40(10):655-660.
88. Elster AD. How much contrast is enough? Dependence of enhancement on field strength and MR pulse sequence. Eur Radiol. 1997;7(suppl 5):276-280.
89. Chang KH, Ra DG, Han MH, et al. Contrast enhancement of brain tumors at different MR field strengths: comparison of 0.5 T and 2.0 T. AJNR Am J Neuroradiol. 1994;15(8):1413-1419.
90. Giesel FL, von Tengg-Kobligk H, Griffiths PD, et al. Effects of field strength and protein content on r1 and r2 of different contrast agents. RSNA. 2005. Book of Abstracts.
91. Krautmacher C, Willinek WA, Tschampa HJ, et al. Brain tumors: full- and half-dose contrast-enhanced MR imaging at 3.0 T compared with 1.5 T - initial experience. Radiology. 2005;237(3):1014-1019.
92. Trattnig S, Pinker K, Ba-Ssalamah A, et al. The optimal use of contrast agents at high field MRI. Eur Radiol. 2006;16(6):1280-1287.
93. Brekenfeld C, Foert E, Hundt W, et al. Enhancement of cerebral diseases: how much contrast agent is enough? Comparison of 0.1, 0.2, and 0.3 mmol/kg gadoteridol at 0.2 T with 0.1 mmol/kg gadoteridol at 1.5 T. Invest Radiol. 2001;36(5):266-275.
94. Runge VM, Gelblum DY, Pacetti ML, et al. Gd-HP-DO3A in clinical MR imaging of the brain. Radiology. 1990;177(2):393-400.
95. Haustein J, Laniado M, Niendorf HP, et al. Triple-dose versus standard-dose gadopentetate dimeglumine: a randomized study in 199 patients. Radiology. 1993;186(3):855-860.
96. Runge VM, Kirsch JE, Burke VJ, et al. High-dose gadoteridol in MR imaging of intracranial neoplasms. J Magn Reson Imaging. 1992;2(1):9-18.
97. Haba D, Pasco PA, Tanguy JY, et al. Use of half-dose gadolinium-enhanced MRI and magnetization transfer saturation in brain tumors. Eur Radiol. 2001;11(1):117-122.
98. Gehl HB, Bourne M, Grazioli L, et al. Off-site evaluation of liver lesion detection by Gd-BOPTA-enhanced MR imaging. Eur Radiol. 2001;11(2):187-192.
99. Petersein J, Spinazzi A, Giovagnoni A, et al. Focal liver lesions: evaluation of the efficacy of gadobenate dimeglumine in MR imaging - a multicenter phase III clinical study. Radiology. 2000;215(3):727-736.
100. Cavagna FM, Maggioni F, Castelli PM, et al. Gadolinium chelates with weak binding to serum proteins. A new class of high-efficiency, general purpose contrast agents for magnetic resonance imaging. Invest Radiol. 1997;32(12):780-796.
101. Runge VM, Armstrong MR, Barr RG, et al. A clinical comparison of the safety and efficacy of MultiHance (gadobenate dimeglumine) and Omniscan (Gadodiamide) in magnetic resonance imaging in patients with central nervous system pathology. Invest Radiol. 2001;36(2):65-71.
102. Colosimo C, Ruscalleda J, Korves M, et al. Detection of intracranial metastases: a multicenter, intrapatient comparison of gadobenate dimeglumine-enhanced MRI with routinely used contrast agents at equal dosage. Invest Radiol. 2001;36(2):72-81.
103. Law M. MR spectroscopy of brain tumors. Top Magn Reson Imaging. 2004;15(5):291-313.
104. Provenzale JM, Mukundan S, Barboriak DP. Diffusion-weighted and perfusion MR imaging for brain tumor characterization and assessment of treatment response. Radiology. 2006;239(3):632-649.
105. Cha S, Knopp EA, Johnson G, et al. Intracranial mass lesions: dynamic contrast-enhanced susceptibility-weighted echo-planar perfusion MR imaging. Radiology. 2002;223(1):11-29.
106. Barbier EL, Lamalle L, Decorps M. Methodology of brain perfusion imaging. J Magn Reson Imaging. 2001;13(4):496-520.
107. Ostergaard L. Principles of cerebral perfusion imaging by bolus tracking. J Magn Reson Imaging. 2005;22(6):710-717.
108. Cha S. Perfusion MR imaging of brain tumors. Top Magn Reson Imaging. 2004;15(5):279-289.
109. Hartmann M, Heiland S, Harting I, et al. Distinguishing of primary cerebral lymphoma from high-grade glioma with perfusion-weighted magnetic resonance imaging. Neurosci Lett. 2003;338(2):119-122.
110. Law M, Yang S, Wang H, et al. Glioma grading: sensitivity, specificity, and predictive values of perfusion MR imaging and proton MR spectroscopic imaging compared with conventional MR imaging. AJNR Am J Neuroradiol. 2003;24(10):1989-1998.
111. Weber MA, Zoubaa S, Schlieter M, et al. Diagnostic performance of spectroscopic and perfusion MRI for distinction of brain tumors. Neurology. 2006;66(12):1899-1906.
112. Law M, Cha S, Knopp EA, et al. High-grade gliomas and solitary metastases: differentiation by using perfusion and proton spectroscopic MR imaging. Radiology. 2002;222(3):715-721.
113. Aronen HJ, Gazit IE, Louis DN, et al. Cerebral blood volume maps of gliomas: comparison with tumor grade and histologic findings. Radiology. 1994;191(1):41-51.
114. Sugahara T, Korogi Y, Tomiguchi S, et al. Posttherapeutic intraaxial brain tumor: the value of perfusion-sensitive contrast-enhanced MR imaging for differentiating tumor recurrence from nonneoplastic contrast-enhancing tissue. AJNR Am J Neuroradiol. 2000;21(5):901-909.
115. Knopp EA, Cha S, Johnson G, et al. Glial neoplasms: dynamic contrast-enhanced T2*-weighted MR imaging. Radiology. 1999;211(3):791-798.
116. Shin JH, Lee HK, Kwun BD, et al. Using relative cerebral blood flow and volume to evaluate the histopathologic grade of cerebral gliomas: preliminary results. AJR Am J Roentgenol. 2002;179(3):783-789.