Advanced magnetic resonance imaging of the physical processes in human Glioblastoma

Cancer Research

Volumn 74, Issue 17, 2014, Pages 4622-4637

  Kalpathy Cramer, Jayashree ^a   Gerstner, Elizabeth R ^a   Emblem, Kyrre E ^a,b   Andronesi, Ovidiu C ^a   Rosen, Bruce ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR MARKER;

BRAIN TUMOR; DIFFUSION WEIGHTED IMAGING; GLIOBLASTOMA; HUMAN; METABOLISM; PATHOLOGY; PHYSICAL PHENOMENA; PROCEDURES;

BRAIN NEOPLASMS; DIFFUSION MAGNETIC RESONANCE IMAGING; GLIOBLASTOMA; HUMANS; PHYSICAL PROCESSES; TUMOR MARKERS, BIOLOGICAL;

EID: 84907053684     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0383     Document Type: Review

References (173)

1. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009;10:459-66.
2. Grossman SA, Ye X, Piantadosi S, Desideri S, Nabors LB, Rosenfeld M, et al. Survival of patients with newly diagnosed glioblastoma treated with radiation and temozolomide in research studies in the United States. Clin Cancer Res 2010;16:2443-9.
3. Lai A, Tran A, Nghiemphu PL, Pope WB, Solis OE, Selch M, et al. Phase II study of bevacizumab plus temozolomide during and after radiation therapy for patients with newly diagnosed glioblastoma multiforme. J Clin Oncol 2011;29:142-8.
4. Dolecek TA, Propp JM, Stroup NE, Kruchko C. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2005-2009. Neuro Oncol 2012;14 Suppl 5:v1-49.
5. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med 2008; 359:492-507.
6. Al-Okaili RN, Krejza J, Wang S, Woo JH, Melhem ER. Advanced MR imaging techniques in the diagnosis of intraaxial brain tumors in adults. Radiographics 2006;26 Suppl 1:S173-89.
7. Pope WB, Sayre J, Perlina A, Villablanca JP, Mischel PS, Cloughesy TF. MR imaging correlates of survival in patients with high-grade gliomas. AJNR Am J Neuroradiol 2005;26:2466-74.
8. Gerstner ER, Chen PJ, Wen PY, Jain RK, Batchelor TT, Sorensen G. Infiltrative patterns of glioblastoma spread detected via diffusion MRI after treatment with cediranib. Neuro Oncol 2010;12: 466-72.
9. Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 2010;28:1963-72.
10. Chinot OL, Macdonald DR, Abrey LE, Zahlmann G, Kerloeguen Y, Cloughesy TF. Response assessment criteria for glioblastoma: practical adaptation and implementation in clinical trials of antiangiogenic therapy. Curr Neurol Neurosci Rep 2013;13:347.
11. Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, Batchelor TT. Angiogenesis in brain tumours. Nat Rev Neurosci 2007;8:610-22.
12. Pries AR, Hopfner M, le Noble F, Dewhirst MW, Secomb TW. The shunt problem: control of functional shunting in normal and tumour vasculature. Nat Rev Cancer 2010;10:587-93.
13. Jain RK. Normalizing tumor microenvironment to treat cancer: bench to bedside to biomarkers. J Clin Oncol 2013;31:2205-18.
14. Guo P, Hu B, Gu W, Xu L, Wang D, Huang HJ, et al. Platelet-derived growth factor-B enhances glioma angiogenesis by stimulating vascular endothelial growth factor expression in tumor endothelia and by promoting pericyte recruitment. Am J Pathol 2003;162:1083-93.
15. Svolos P, Tsolaki E, Kapsalaki E, Theodorou K, Fountas K, Fezoulidis I, et al. Investigating brain tumor differentiation with diffusion and perfusion metrics at 3T MRI using pattern recognition techniques. Magn Reson Imaging 2013;31:1567-77.
16. Young GS. Advanced MRI of adult brain tumors. Neurol Clin 2007; 25:947-73.
17. Jain R, Griffith B, Narang J, Mikkelsen T, Bagher-Ebadian H, Nejad- Davarani SP, et al. Blood-brain-barrier imaging in brain tumors: concepts and methods. Neurographics 2012;2:48-59.
18. Ellingson BM, Cloughesy TF, Lai A, Nghiemphu PL, Pope WB. Cell invasion, motility, and proliferation level estimate (CIMPLE) maps derived from serial diffusion MR images in recurrent glioblastoma treated with bevacizumab. J Neurooncol 2011;105:91-101.
19. Gerstner ER, Sorensen AG. Diffusion and diffusion tensor imaging in brain cancer. Semin Radiat Oncol 2011;21:141-6.
20. Farrar CT, Kamoun WS, Ley CD, Kim YR, Kwon SJ, Dai G, et al. In vivo validation of MRI vessel caliber index measurement methods with intravital optical microscopy in a U87 mouse brain tumor model. Neuro Oncol 2010;12:341-50.
21. Hamstra DA, Rehemtulla A, Ross BD. Diffusion magnetic resonance imaging: a biomarker for treatment response in oncology. J Clin Oncol 2007;25:4104-9.
22. Chenevert TL, Stegman LD, Taylor JM, Robertson PL, GreenbergHS, Rehemtulla A, et al. Diffusion magnetic resonance imaging: an early surrogate marker of therapeutic efficacy in brain tumors. J Natl Cancer Inst 2000;92:2029-36.
23. Provenzale JM, Mukundan S, Barboriak DP. Diffusion-weighted and perfusion MR imaging for brain tumor characterization and assessment of treatment response. Radiology 2006;239:632-49.
24. Batchelor TT, Gerstner ER, Emblem KE, Duda DG, Kalpathy-Cramer J, Snuderl M, et al. Improved tumor oxygenation and survival in glioblastoma patients who show increased blood perfusion after cediranib and chemoradiation. Proc Natl Acad Sci U S A 2013;110: 19059-64.
25. Sorensen AG, Batchelor TT, Zhang WT, Chen PJ, Yeo P, Wang M, et al. A "vascular normalization index" as potential mechanistic biomarker to predict survival after a single dose of cediranib in recurrent glioblastoma patients. Cancer Res 2009;69:5296-300.
26. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005;307:58-62.
27. Sorensen AG, Emblem KE, Polaskova P, Jennings D, Kim H, Ancukiewicz M, et al. Increased survival of glioblastoma patients who respond to antiangiogenic therapy with elevated blood perfusion. Cancer Res 2012;72:402-7.
28. Goel S, Duda DG, Xu L, Munn LL, Boucher Y, Fukumura D, et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev 2011;91:1071-121.
29. Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, Duda DG, Cohen KS, et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007;11:83-95.
30. Padhani AR, Leach MO. Antivascular cancer treatments: functional assessments by dynamic contrast-enhanced magnetic resonance imaging. Abdom Imaging 2005;30:324-41.
31. Emblem KE, Zoellner FG, Tennoe B, Nedregaard B, Nome T, Due- Tonnessen P, et al. Predictive modeling in glioma grading from MR perfusion images using support vector machines. Magn Reson Med 2008;60:945-52.
32. Padhani AR, Miles KA. Multiparametric imaging of tumor response to therapy. Radiology 2010;256:348-64.
33. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, et al. IDH1 and IDH2 mutations in gliomas.NEngl JMed 2009;360:765-73.
34. Lee EQ, Kuhn J, Lamborn KR, Abrey L, DeAngelis LM, Lieberman F, et al. Phase I/II study of sorafenib in combination with temsirolimus for recurrent glioblastoma or gliosarcoma: North American Brain Tumor Consortium study 05-02. Neuro Oncol 2012;14:1511-8.
35. Peereboom DM, Ahluwalia MS, Ye X, Supko JG, Hilderbrand SL, Phuphanich S, et al. NABTT 0502: a phase II and pharmacokinetic study of erlotinib and sorafenib for patients with progressive or recurrent glioblastoma multiforme. Neuro Oncol 2013;15:490-6.
36. Batchelor TT, Mulholland P, Neyns B, Nabors LB, Campone M, Wick A, et al. Phase III randomized trial comparing the efficacy of cediranib as monotherapy, and in combination with lomustine, versus lomustine alone in patients with recurrent glioblastoma. J Clin Oncol 2013;31:3212-8.
37. Parker GJM, Padhani AR. T1-W DCE-MRI: T1-Weighted Dynamic Contrast-Enhanced MRI. In: Tofts P, editor. Quantitative MRI of the Brain. Chichester, UK: John Wiley &Sons, Ltd; 2003.
38. Stevenson VL, Parker GJ, Barker GJ, Birnie K, Tofts PS, Miller DH, et al. Variations in T1 and T2 relaxation times of normal appearing white matter and lesions in multiple sclerosis. J Neurol Sci 2000; 178:81-7.
39. Jain RK, Booth MF. What brings pericytes to tumor vessels? J Clin Invest 2003;112:1134-6.
40. Tofts PS, Brix G, Buckley DL, Evelhoch JL, Henderson E, Knopp MV, et al. Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols. J Magn Reson Imaging 1999;10:223-32.
41. Parker GJ, Tofts PS. Pharmacokinetic analysis of neoplasms using contrast-enhanced dynamic magnetic resonance imaging. Top Magn Reson Imaging 1999;10:130-42.
42. Jackson A. Imaging microvascular structure with contrast enhanced MRI. Br J Radiol 2003;76:S159-73.
43. Harrer JU, Parker GJ, Haroon HA, Buckley DL, Embelton K, Roberts C, et al. Comparative study of methods for determining vascular permeability and blood volume in human gliomas. J Magn Reson Imaging 2004;20:748-57.
44. Jackson A. Analysis of dynamic contrast enhanced MRI. Br J Radiol 2004;77 Spec No 2:S154-66.
45. Collins DJ, Padhani AR. Dynamic magnetic resonance imaging of tumor perfusion. Approaches and biomedical challenges. IEEE Eng Med Biol Mag 2004;23:65-83.
46. Roberts C, Issa B, Stone A, Jackson A, Waterton JC, Parker GJ. Comparative study into the robustness of compartmental modeling and model-free analysis in DCE-MRI studies. J Magn Reson Imaging 2006;23:554-63.
47. Jackson A, O'Connor JP, Parker GJ, Jayson GC. Imaging tumor vascular heterogeneity and angiogenesis using dynamic contrastenhanced magnetic resonance imaging. Clin Cancer Res 2007;13: 3449-59.
48. O'Connor JP, Jackson A, Asselin MC, Buckley DL, Parker GJ, Jayson GC. Quantitative imaging biomarkers in the clinical development of targeted therapeutics: current and future perspectives. Lancet Oncol 2008;9:766-76.
49. Barboriak DP, MacFall JR, Viglianti BL, Dewhirst Dvm MW. Comparison of three physiologically-based pharmacokinetic models for the prediction of contrast agent distribution measured by dynamic MR imaging. J Magn Reson Imaging 2008;27:1388-98.
50. Patlak CS, Blasberg RG, Fenstermacher JD. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. J Cereb Blood Flow Metab 1983;3:1-7.
51. Ferl GZ, Xu L, Friesenhahn M, Bernstein LJ, Barboriak DP, Port RE. An automated method for nonparametric kinetic analysis of clinical DCEMRI data: application to glioblastoma treated with bevacizumab. Magn Reson Med 2010;63:1366-75.
52. Parker GJM, Suckling J, Tanner SF, Padhani AR, Revell PB, Husband JE, et al. Probing tumor microvascularity by measurement, analysis and display of contrast agent uptake kinetics. J Magn Reson Imaging 1997;7:564-74.
53. Tofts PS. Modeling tracer kinetics in dynamic Gd-DTPA MR imaging. J Magn Reson Imaging 1997;7:91-101.
54. Sourbron SP, Buckley DL. On the scope and interpretation of the Tofts models for DCE-MRI. Magn Reson Med 2011;66:735-45.
55. Schenck JF. The role of magnetic susceptibility in magnetic resonance imaging: MRI magnetic compatibility of the first and second kinds. Med Phys 1996;23:815-50.
56. Rosen BR, Belliveau JW, Vevea JM, Brady TJ. Perfusion imaging with NMR contrast agents. Magn Reson Med 1990;14:249-65.
57. Belliveau JW, Rosen BR, Kantor HL, Rzedzian RR, Kennedy DN, McKinstry RC, et al. Functional cerebral imaging by susceptibilitycontrast NMR. Magn Reson Med 1990;14:538-46.
58. Rosen BR, Belliveau JW, Aronen HJ, Kennedy D, Buchbinder BR, Fischman A, et al. Susceptibility contrast imaging of cerebral blood volume: human experience. Magn Reson Med 1991;22:293-9.
59. Meier P, Zierler KL. On the theory of the indicator-dilution method for measurement of blood flow and volume. J Appl Physiol 1954;6:731-44.
60. Zaharchuk G. Theoretical basis of hemodynamic MR imaging techniques to measure cerebral blood volume, cerebral blood flow, and permeability. AJNR Am J Neuroradiol 2007;28:1850-8.
61. Ostergaard L, Weisskoff RM, Chesler DA, Gyldensted C, Rosen BR. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis. Magn Reson Med 1996;36:715-25.
62. Cha S, Knopp EA, Johnson G, Wetzel SG, Litt AW, Zagzag D. Intracranial mass lesions: dynamic contrast-enhanced susceptibility- weighted echo-planar perfusion MR imaging. Radiology 2002; 223:11-29.
63. van Osch MJ, Vonken EJ, Bakker CJ, Viergever MA. Correcting partial volume artifacts of the arterial input function in quantitative cerebral perfusion MRI. Magn Reson Med 2001;45:477-85.
64. Fisel CR, Ackerman JL, Buxton RB, Garrido L, Belliveau JW, Rosen BR, et al. MR contrast due to microscopically heterogeneous magnetic susceptibility: numerical simulations and applications to cerebral physiology. Magn Reson Med 1991;17:336-47.
65. Rosen BR, Belliveau JW, Buchbinder BR, McKinstry RC, Porkka LM, Kennedy DN, et al. Contrast agents and cerebral hemodynamics. Magn Reson Med 1991;19:285-92.
66. Weisskoff RM, Zuo CS, Boxerman JL, Rosen BR. Microscopic susceptibility variation and transverse relaxation: theory and experiment. Magn Reson Med 1994;31:601-10.
67. Boxerman JL, Hamberg LM, Rosen BR, Weisskoff RM.MRcontrast due to intravascular magnetic susceptibility perturbations. Magn Reson Med 1995;34:555-66.
68. Dennie J, Mandeville JB, Boxerman JL, Packard SD, Rosen BR, Weisskoff RM.NMRimaging of changes in vascular morphology due to tumor angiogenesis. Magn Reson Med 1998;40:793-9.
69. Einstein A. [Uber die von der molekularkinetischen Theorie der Wärme geforderte Bewegung von in ruhenden Flüssigkeiten suspendierten Teilchen]. Annalen der Physik 1905;322:549-60.
70. Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 2001;13:534-46.
71. Hagmann P, Jonasson L, Maeder P, Thiran J-P, Wedeen VJ, Meuli R. Understanding diffusion MR imaging techniques: from scalar diffusion- weighted imaging to diffusion tensor imaging and beyond. Radiographics 2006;26:S205-23.
72. Le Bihan D, Johansen-Berg H. Diffusion MRI at 25: exploring brain tissue structure and function. Neuroimage 2012;61:324-41.
73. Chenevert T, McKeever P, Ross B. Monitoring early response of experimental brain tumors to therapy using diffusion magnetic resonance imaging. Clin Cancer Res 1997;3:1457-66.
74. Chenevert TL, Ross BD. Diffusion imaging for therapy response assessment of brain tumor. Neuroimaging Clin N Am 2009;19:559-71.
75. Chenevert TL, Sundgren PC, Ross BD. Diffusion imaging: insight to cell status and cytoarchitecture. Neuroimaging Clin N Am 2006; 16:619-32, viii-ix.
76. Negendank W. Studies of human tumors by MRS: a review. NMR Biomed 1992;5:303-24.
77. Kauppinen RA, Peet AC. Using magnetic resonance imaging and spectroscopy in cancer diagnostics and monitoring preclinical and clinical approaches. Cancer Biol Ther 2011;12:665-79.
78. Nelson SJ. Multivoxel magnetic resonance spectroscopy of brain tumors. Mol Cancer Ther 2003;2:497-507.
79. Bluml S, Moreno-Torres A, Shic F, Nguy CH, Ross BD. Tricarboxylic acid cycle of glia in the in vivo human brain. NMR Biomed 2002; 15:1-5.
80. Mora B, Narasimhan PT, Ross BD, Allman J, Barker PB. 31Psaturation transfer and phosphocreatine imaging in the monkey brain. Proc Natl Acad Sci U S A 1991;88:8372-6.
81. Wijnen JP, Van der Graaf M, Scheenen TW, Klomp DW, de Galan BE, Idema AJ, et al. In vivo 13C magnetic resonance spectroscopy of a human brain tumor after application of 13C-1-enriched glucose.Magn Reson Imaging 2010;28:690-7.
82. Lanz B, Xin L, Millet P, Gruetter R. In vivo quantification of neuro-glial metabolism and glial glutamate concentration using (1) H-[(13) C] MRS at 14.1T. J Neurochem 2014;128:125-39.
83. Park JM, Josan S, Grafendorfer T, Yen YF, Hurd RE, Spielman DM, et al. Measuring mitochondrial metabolism in rat brain in vivo using MR Spectroscopy of hyperpolarized [2-(1)(3)C]pyruvate. NMR Biomed 2013;26:1197-203.
84. Bohndiek SE, Kettunen MI, Hu DE, Witney TH, Kennedy BW, Gallagher FA, et al. Detection of tumor response to a vascular disrupting agent by hyperpolarized 13C magnetic resonance spectroscopy. Mol Cancer Ther 2010;9:3278-88.
85. Park I, Larson PE, Zierhut ML, Hu S, Bok R, Ozawa T, et al. Hyperpolarized 13C magnetic resonance metabolic imaging: application to brain tumors. Neuro Oncol 2010;12:133-44.
86. Ward CS, Venkatesh HS, Chaumeil MM, Brandes AH, Vancriekinge M, Dafni H, et al. Noninvasive detection of target modulation following phosphatidylinositol 3-kinase inhibition using hyperpolarized 13C magnetic resonance spectroscopy. Cancer Res 2010;70:1296-305.
87. Warren WS, Jenista E, Branca RT, Chen X. Increasing hyperpolarized spin lifetimes through true singlet eigenstates. Science 2009; 323:1711-4.
88. Pileio G1, Bowen S, Laustsen C, Tayler MC, Hill-Cousins JT, Brown LJ, Brown RC, Ardenkjaer-Larsen JH, Levitt MH. Recycling and imaging of nuclear singlet hyperpolarization. J Am Chem Soc 2013; 135:5084-8.
89. Griffin JL, Shockcor JP. Metabolic profiles of cancer cells. Nat Rev Cancer 2004;4:551-61.
90. Dowling C, Bollen AW, Noworolski SM, McDermottMW,Barbaro NM, Day MR, et al. Preoperative proton MR spectroscopic imaging of brain tumors: correlation with histopathologic analysis of resection specimens. Am J Neuroradiol 2001;22:604-12.
91. Nelson SJ. Assessment of therapeutic response and treatment planning for brain tumors using metabolic and physiological MRI. NMR Biomed 2011;24:734-49.
92. Hamstra DA, Lee KC, Tychewicz JM, Schepkin VD, Moffat BA, Chen M, et al. The use of 19F spectroscopy and diffusion-weighted MRI to evaluate differences in gene-dependent enzyme prodrug therapies. Mol Ther 2004;10:916-28.
93. Clarke JL, Chang S. Pseudoprogression and pseudoresponse: challenges in brain tumor imaging. Curr Neurol Neurosci Rep 2009;9: 241-6.
94. Batchelor TT, Duda DG, di Tomaso E, Ancukiewicz M, Plotkin SR, Gerstner E, et al. Phase II study of cediranib, an oral pan-vascular endothelial growth factor receptor tyrosine kinase inhibitor, in patients with recurrent glioblastoma. J Clin Oncol 2010;28:2817-23.
95. Maia AC Jr, Malheiros SM, da Rocha AJ, Stavale JN, Guimaraes IF, Borges LR, et al. Stereotactic biopsy guidance in adults with supratentorial nonenhancing gliomas: role of perfusion-weighted magnetic resonance imaging. J Neurosurg 2004;101:970-6.
96. Lev MH, Ozsunar Y, Henson JW, Rasheed AA, Barest GD, Harsh GRt, et al. 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. AJNR Am J Neuroradiol 2004;25:214-21.
97. Covarrubias DJ, Rosen BR, Lev MH. Dynamic magnetic resonance perfusion imaging of brain tumors. Oncologist 2004;9:528-37.
98. LawM, Yang S, Wang H, Babb JS, JohnsonG,Cha S, 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: 1989-98.
99. Law M, Yang S, Babb JS, Knopp EA, Golfinos JG, Zagzag D, et al. Comparison of cerebral blood volume and vascular permeability from dynamic susceptibility contrast-enhanced perfusion MR imaging with glioma grade. AJNR Am J Neuroradiol 2004;25:746-55.
100. Law M, Young R, Babb J, Rad M, Sasaki T, Zagzag D, et al. 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 2006;27:1975-82.
101. Boxerman JL, Schmainda KM, Weisskoff RM. 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 2006;27:859-67.
102. Danchaivijitr N, Waldman AD, Tozer DJ, Benton CE, Brasil Caseiras G, Tofts PS, et al. Low-grade gliomas: do changes in rCBV measurements at longitudinal perfusion-weighted MR imaging predict malignant transformation? Radiology 2008;247:170-8.
103. Ludemann L, Grieger W, Wurm R, Budzisch M, Hamm B, Zimmer C. Comparison of dynamic contrast-enhanced MRI with WHO tumor grading for gliomas. Eur Radiol 2001;11:1231-41.
104. Awasthi R, Rathore RK, Soni P, Sahoo P, Awasthi A, Husain N, et al. Discriminant analysis to classify glioma grading using dynamic contrast- enhanced MRI and immunohistochemical markers. Neuroradiology 2012;54:205-13.
105. Liu X, Tian W, Kolar B, Yeaney GA, Qiu X, Johnson MD, et al. MR diffusion tensor and perfusion-weighted imaging in preoperative grading of supratentorial nonenhancing gliomas. Neuro Oncol 2011;13:447-55.
106. Byrnes TJ, Barrick TR, Bell BA, Clark CA. Diffusion tensor imaging discriminates between glioblastoma and cerebral metastases in vivo. NMR Biomed 2011;24:54-60.
107. Nimsky C,Ganslandt O, Hastreiter P,Wang R,Benner T, Sorensen AG, et al. Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery 2007;61:178-85.
108. Kekhia H, Rigolo L, Norton I, Golby AJ. Special surgical considerations for functional brain mapping. Neurosurg Clin N Am 2011; 22:111-32, vii.
109. Crisi G, Orsingher L, Filice S. Lipid and macromolecules quantitation in differentiating glioblastoma from solitary metastasis: a short-echo time single-voxel magnetic resonance spectroscopy study at 3 T. J Comput Assist Tomogr 2013;37:265-71.
110. Tsougos I, Svolos P, Kousi E, Fountas K, Theodorou K, Fezoulidis I, et al. Differentiation of glioblastoma multiforme from metastatic brain tumor using proton magnetic resonance spectroscopy, diffusion and perfusion metrics at 3 T. Cancer Imaging 2012;12:423-36.
111. Ellingson BM, Malkin MG, Rand SD, Connelly JM, Quinsey C, LaViolette PS, et al. Validation of functional diffusion maps (fDMs) as a biomarker for human glioma cellularity. J Magn Reson Imaging 2010; 31:538-48.
112. Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, Hirai T, et al. Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 1999;9:53-60.
113. Aref M, Chaudhari AR, Bailey KL, Aref S, Wiener EC. Comparison of tumor histology to dynamic contrast enhanced magnetic resonance imaging-based physiological estimates. Magn Reson Imaging 2008; 26:1279-93.
114. Aryal MP, Nagaraja TN, Keenan KA, Bagher-Ebadian H, Panda S, Brown SL, et al. Dynamic contrast enhanced MRI parameters and tumor cellularity in a rat model of cerebral glioma at 7 T. Magn Reson Med 2014;71:2206-14.
115. Swanson KR, Rostomily RC, Alvord EC Jr. A mathematical modelling tool for predicting survival of individual patients following resection of glioblastoma: a proof of principle. Br J Cancer 2008;98:113-9.
116. Hawkins-Daarud A, Rockne RC, Anderson AR, Swanson KR. Modeling tumor-associated edema in gliomas during anti-angiogenic therapy and its impact on imageable tumor. Front Oncol 2013;3:66.
117. Wang CH, Rockhill JK, Mrugala M, Peacock DL, Lai A, Jusenius K, et al. Prognostic significance of growth kinetics in newly diagnosed glioblastomas revealed by combining serial imaging with a novel biomathematical model. Cancer Res 2009;69:9133-40.
118. Swanson KR, Rockne RC, Claridge J, Chaplain MA, Alvord EC Jr, Anderson AR. Quantifying the role of angiogenesis in malignant progression of gliomas: in silico modeling integrates imaging and histology. Cancer Res 2011;71:7366-75.
119. Alvord EC, Swanson KR. Using mathematical modeling to predict survival of low-grade gliomas. Ann Neurol 2007;61:496.
120. Swanson KR, Harpold HL, Peacock DL, Rockne R, Pennington C, Kilbride L, et al. Velocity of radial expansion of contrast-enhancing gliomas and the effectiveness of radiotherapy in individual patients: a proof of principle. Clin Oncol 2008;20:301-8.
121. Swanson KR, Bridge C, Murray JD, Alvord J, Ellsworth C. Virtual and real brain tumors: using mathematical modeling to quantify glioma growth and invasion. J Neurol Sci 2003;216:1-10.
122. Corwin D, Holdsworth C, Rockne RC, Trister AD, Mrugala MM, Rockhill JK, et al. Toward patient-specific, biologically optimized radiation therapy plans for the treatment of glioblastoma. PLoS ONE 2013;8:e79115.
123. Zou P, Xu H, Chen P, Yan Q, Zhao L, Zhao P, et al. IDH1/IDH2 mutations define the prognosis and molecular profiles of patientswith gliomas: a meta-analysis. PloS ONE 2013;8:e68782.
124. Cohen AL, Holmen SL, Colman H. IDH1 and IDH2 mutations in gliomas. Curr Neurol Neurosci Rep 2013;13:345.
125. Weller M, Wick W, von Deimling A. Isocitrate dehydrogenase mutations: a challenge to traditional views on the genesis and malignant progression of gliomas. Glia 2011;59:1200-4.
126. Houillier C, Wang X, Kaloshi G, Mokhtari K, Guillevin R, Laffaire J, et al. IDH1 or IDH2 mutations predict longer survival and response to temozolomide in low-grade gliomas. Neurology 2010; 75:1560-6.
127. Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 2010;465:966.
128. Andronesi OC, Kim GS, Gerstner E, Batchelor T, Tzika AA, Fantin VR, et al. Detection of 2-hydroxyglutarate in IDH-mutated glioma patients by in vivo spectral-editing and 2D correlation magnetic resonance spectroscopy. Sci Transl Med 2012;4:116ra4.
129. Choi C, Ganji SK, DeBerardinis RJ, Hatanpaa KJ, Rakheja D, Kovacs Z, et al. 2-hydroxyglutarate detection by magnetic resonance spectroscopy in IDH-mutated patients with gliomas. Nat Med 2012; 18:624-9.
130. Andronesi OC, Rapalino O, Gerstner E, Chi A, Batchelor TT, Cahill DP, et al. Detection of oncogenic IDH1 mutations using magnetic resonance spectroscopy of 2-hydroxyglutarate. J Clin Invest 2013;123: 3659-63.
131. Tykocinski ES, Grant RA, Kapoor GS, Krejza J, Bohman LE, Gocke TA, et al. Use of magnetic perfusion-weighted imaging to determine epidermal growth factor receptor variant III expression in glioblastoma. Neuro Oncol 2012;14:613-23.
132. Diehn M, Nardini C, Wang DS, McGovern S, Jayaraman M, Liang Y, et al. Identification of noninvasive imaging surrogates for brain tumor gene-expression modules. Proc Natl Acad Sci U S A 2008;105: 5213-8.
133. Young RJ, Gupta A, Shah AD, Graber JJ, Schweitzer AD, Prager A, et al. Potential role of preoperative conventional MRI including diffusion measurements in assessing epidermal growth factor receptor gene amplification status in patients with glioblastoma. AJNR Am J Neuroradiol 2013;34:2271-7.
134. Macdonald DR, Cascino TL, Schold SC Jr, Cairncross JG. Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol 1990;8:1277-80.
135. Hamstra DA, Chenevert TL, Moffat BA, Johnson TD, Meyer CR, Mukherji SK, et al. Evaluation of the functional diffusion map as an early biomarker of time-to-progression and overall survival in high-grade glioma. Proc Natl Acad Sci U S A 2005;102: 16759-64.
136. Ellingson BM, Cloughesy TF, Lai A, Nghiemphu PL, Pope WB. Nonlinear registration of diffusion-weighted images improves clinical sensitivity of functional diffusion maps in recurrent glioblastoma treated with bevacizumab. Magn Reson Med 2012; 67:237-45.
137. Ellingson BM, Cloughesy TF, Lai A, Mischel PS, Nghiemphu PL, Lalezari S, et al. Graded functional diffusion map-defined characteristics of apparent diffusion coefficients predict overall survival in recurrent glioblastoma treated with bevacizumab. Neuro Oncol 2011;13:1151-61.
138. Tsien C, Galban CJ, Chenevert TL, Johnson TD, Hamstra DA, Sundgren PC, et al. Parametric response map as an imaging biomarker to distinguish progression from pseudoprogression in highgrade glioma. J Clin Oncol 2010;28:2293-9.
139. Galban CJ, Chenevert TL, Meyer CR, Tsien C, Lawrence TS, Hamstra DA, et al. Prospective analysis of parametric response map-derived MRI biomarkers: identification of early and distinct glioma response patterns not predicted by standard radiographic assessment. Clin Cancer Res 2011;17:4751-60.
140. Galban CJ, Chenevert TL, Meyer CR, Tsien C, Lawrence TS, Hamstra DA, et al. The parametric response map is an imaging biomarker for early cancer treatment outcome. Nat Med 2009;15:572-6.
141. Kiselev VG, Strecker R, Ziyeh S, Speck O, Hennig J. Vessel size imaging in humans. Magn Reson Med 2005;53:553-63.
142. Emblem KE, Mouridsen K, Bjornerud A, Farrar CT, Jennings D, Borra RJ, et al. Vessel architectural imaging identifies cancer patient responders to anti-angiogenic therapy. Nat Med 2013;19:1178-83.
143. Xu C, Kiselev VG, Moller HE, Fiebach JB. Dynamic hysteresis between gradient echo and spin echo attenuations in dynamic susceptibility contrast imaging. Magn Reson Med 2013;69:981-91.
144. Pinho MC, Polaskova P, Kalpathy-Cramer J, Jennings D, Emblem KE, Jain RK, et al. Low incidence of pseudoprogression by imaging in newly diagnosed glioblastoma patients treated with cediranib in combination with chemoradiation. Oncologist 2014;19:75-81.
145. Shah R, Vattoth S, Jacob R, Manzil FFP, O'Malley JP, Borghei P, et al. Radiation necrosis in the brain: imaging features and differentiation from tumor recurrence. Radiographics 2012;32:1343-59.
146. Verma N, Cowperthwaite MC, Burnett MG, Markey MK. Differentiating tumor recurrence from treatment necrosis: a review of neurooncologic imaging strategies. Neuro Oncol 2013;15:515-34.
147. Brandes AA, Tosoni A, Spagnolli F, Frezza G, Leonardi M, Calbucci F, et al. Disease progression or pseudoprogression after concomitant radiochemotherapy treatment: pitfalls in neurooncology. Neuro Oncol 2008;10:361-7.
148. Van Mieghem E, Wozniak A, Geussens Y, Menten J,De Vleeschouwer S, Van Calenbergh F, et al. Defining pseudoprogression in glioblastoma multiforme. Eur J Neurol 2013;20:1335-41.
149. Brandsma D, van den Bent MJ. Pseudoprogression and pseudoresponse in the treatment of gliomas. Curr Opin Neurol 2009;22:633-8.
150. Brandes AA, Franceschi E, Tosoni A, Blatt V, Pession A, Tallini G, et al. MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients. J Clin Oncol 2008; 26:2192-7.
151. de Wit MCY, de Bruin HG, Eijkenboom W, Sillevis Smitt PAE, van den Bent MJ. Immediate post-radiotherapy changes in malignant glioma can mimic tumor progression. Neurology 2004;63:535-7.
152. Gerstner ER, McNamara MB, Norden AD, Lafrankie D, Wen PY. Effect of adding temozolomide to radiation therapy on the incidence of pseudo-progression. J Neurooncol 2009;94:97-101.
153. Taal W, Brandsma D, de Bruin HG, Bromberg JE, Swaak-Kragten AT, Smitt PAES, et al. Incidence of early pseudo-progression in a cohort of malignant glioma patients treated with chemoirradiation with temozolomide. Cancer 2008;113:405-10.
154. Gasparetto EL, Pawlak MA, Patel SH, Huse J, Woo JH, Krejza J, et al. Posttreatment recurrence of malignant brain neoplasm: accuracy of relative cerebral blood volume fraction in discriminating low from high malignant histologic volume fraction. Radiology 2009;250:887-96.
155. Hu LS, Eschbacher JM, Heiserman JE, Dueck AC, Shapiro WR, Liu S, et al. Reevaluating the imaging definition of tumor progression: perfusion MRI quantifies recurrent glioblastoma tumor fraction, pseudoprogression, and radiation necrosis to predict survival. Neuro Oncol 2012;14:919-30.
156. Park I, Tamai G, Lee MC, Chuang CF, Chang SM, Berger MS, et al. Patterns of recurrence analysis in newly diagnosed glioblastoma multiforme after three-dimensional conformal radiation therapy with respect to pre-radiation therapy magnetic resonance spectroscopic findings. Int J Radiat Oncol Biol Phys 2007;69:381-9.
157. Li Y, Lupo JM, Parvataneni R, Lamborn KR, Cha S, Chang SM, et al. Survival analysis in patients with newly diagnosed glioblastoma using pre- and postradiotherapy MR spectroscopic imaging. Neuro Oncol 2013;15:607-17.
158. Gupta A, Young RJ, Karimi S, Sood S, Zhang Z, Mo Q, et al. Isolated diffusion restriction precedes the development of enhancing tumor in a subset of patients with glioblastoma. AJNR Am J Neuroradiol 2011;32:1301-6.
159. Rieger J, Bahr O, Muller K, Franz K, Steinbach J, Hattingen E. Bevacizumab-induced diffusion-restricted lesions in malignant glioma patients. J Neurooncol 2010;99:49-56.
160. Van Cauter S, Veraart J, Sijbers J, Peeters RR, Himmelreich U, De Keyzer F, et al. Gliomas: diffusion kurtosis MR imaging in grading. Radiology 2012;263:492-501.
161. Kothari PD, White NS, Farid N, Chung R, Kuperman JM, Girard HM, et al. Longitudinal restriction spectrum imaging is resistant to pseudoresponse in patients with high-grade gliomas treated with bevacizumab. AJNR Am J Neuroradiol 2013;34:1752-7.
162. Farid N, Almeida-Freitas DB, White NS, McDonald CR, Muller KA, Vandenberg SR, et al. Restriction-spectrum imaging of bevacizumab- related necrosis in a patient with GBM. Front Oncol 2013; 3:258.
163. Assaf Y, Freidlin RZ, Rohde GK, Basser PJ. New modeling and experimental framework to characterize hindered and restricted water diffusion in brain white matter. Magn Reson Med 2004;52:965-78.
164. Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 2005; 53:1432-40.
165. White NS, Leergaard TB, D'Arceuil H, Bjaalie JG, Dale AM. Probing tissue microstructure with restriction spectrum imaging: Histological and theoretical validation. Hum Brain Mapp 2013;34:327-46.
166. Panagiotaki E, Schneider T, Siow B, Hall MG, Lythgoe MF, Alexander DC. Compartment models of the diffusion MR signal in brain white matter: a taxonomy and comparison. Neuroimage 2012; 59:2241-54.
167. Correia Carreira G, Gemeinhardt O, GorenfloR, Beyersdorff D, Franiel T, Plendl J, et al. Limitations of the permeability-limited compartment model in estimating vascular permeability and interstitial volume fraction in DCE-MRI. Magn Reson Imaging 2011;29:639-49.
168. Hassid Y, Furman-Haran E, Margalit R, Eilam R, Degani H. Noninvasive magnetic resonance imaging of transport and interstitial fluid pressure in ectopic human lung tumors. Cancer Res 2006;66: 4159-66.
169. Pellerin M, Yankeelov TE, Lepage M. Incorporating contrast agent diffusion into the analysis of DCE-MRI data. Magn Reson Med 2007;58:1124-34.
170. Yankeelov TE, Rooney WD, Huang W, Dyke JP, Li X, Tudorica A, et al. Evidence for shutter-speed variation in CR bolus-tracking studies of human pathology. NMR Biomed 2005;18:173-85.
171. Carreira GC, Gemeinhardt O, Gorenflo R, Beyersdorff D, Franiel T, Plendl J, et al. Limitations of the permeability-limited compartment model in estimating vascular permeability and interstitial volume fraction in DCE-MRI. Magn Reson Imaging 2011;29:639-49.
172. Mills SJ, Soh C, Rose CJ, Cheung S, Zhao S, Parker GJ, et al. Candidate biomarkers of extravascular extracellular space: a direct comparison of apparent diffusion coefficient and dynamic contrastenhanced MR imaging-derived measurement of the volume of the extravascular extracellular space in glioblastoma multiforme. AJNR Am J Neuroradiol 2010;31:549-53.
173. Paulson ES, Schmainda KM. Comparison of dynamic susceptibilityweighted contrast-enhanced MR methods: recommendations for measuring relative cerebral blood volume in brain tumors. Radiology 2008;249:601-13.