White matter and deep gray matter hemodynamic changes in multiple sclerosis patients with clinically isolated syndrome

Magnetic Resonance in Medicine

Volumn 68, Issue 6, 2012, Pages 1932-1942

  Papadaki, Efrosini Z ^a   Mastorodemos, Vasileios C ^a   Amanakis, Emmanouil Z ^a   Tsekouras, Konstantinos C ^a   Papadakis, Antonis E ^a   Tsavalas, Nikolaos D ^a   Simos, Panagiotis G ^b   Karantanas, Apostolos H ^a   Plaitakis, Andreas ^a   Maris, Thomas G ^a  

^a UNIVERSITY HOSPITAL OF HERAKLION   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

Author keywords

clinically isolated syndrome; dynamic susceptibility contrast perfusion MRI; multiple sclerosis

Indexed keywords

HEMODYNAMICS; MAGNETIC RESONANCE IMAGING; MAGNETIC SUSCEPTIBILITY;

CEREBRAL BLOOD FLOW; CEREBRAL BLOOD VOLUME; CLINICALLY ISOLATED SYNDROME; DYNAMIC SUSCEPTIBILITY CONTRAST MAGNETIC RESONANCE IMAGING; HEMODYNAMIC CHANGES; MULTIPLE SCLEROSIS; PERFUSION MRI; RELAPSING-REMITTING MULTIPLE SCLEROSIS;

BLOOD;

GADOBUTROL;

ADOLESCENT; ADULT; ARTICLE; BRAIN BLOOD FLOW; BRAIN SIZE; CAUDATE NUCLEUS; CENTER FOR EPIDEMIOLOGICAL STUDIES DEPRESSION SCALE; CLINICAL ARTICLE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DEEP GRAY MATTER; DEMYELINATING DISEASE; DENTATE GYRUS; DISEASE EXACERBATION; EXPANDED DISABILITY STATUS SCALE; FEMALE; FUNCTIONAL NEUROIMAGING; GRAY MATTER; HEMODYNAMICS; HIPPOCAMPUS; HUMAN; IMAGE ANALYSIS; MALE; MULTIPLE SCLEROSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTIC NEURITIS; PUTAMEN; RELAPSE; THALAMUS; WHITE MATTER;

EID: 84870057490     PISSN: 07403194     EISSN: 15222594     Source Type: Journal    
DOI: 10.1002/mrm.24194     Document Type: Article

References (59)

1. Miller D, Barkhof F, Montalban X, Thompson A, Filippi M,. Clinically isolated syndromes suggestive of multiple sclerosis, part 1: natural history, pathogenesis, diagnosis, and prognosis. Lancet Neurol 2005; 4: 281-288.
2. Rot U, Mesec A,. Clinical, MRI, CSF and electrophysiological findings in different stages of multiple sclerosis. Clin Neurol Neurosurg 2006; 108: 271-274.
3. Miller DH, Weinshenker BG, Filippi M, Banwell BL, Cohen JA, Freedman MS, Galetta SL, Hutchinson M, Johnson RT, Kappos L, Kira J, Lublin FD, McFarland HF, Montalban X, Panitch H, Richert JR, Reingold SC, Polman CH,. Differential diagnosis of suspected multiple sclerosis: a consensus approach. Mult Scler 2008; 14: 1157-1174.
4. Barkhof F, Filippi M, Miller DH, Scheltens P, Campi A, Polman CH, Comi G, Ade'r HJ, Losseff N, Valk J,. Comparison of MRI criteria at first presentation to predict conversion to clinically definite multiple sclerosis. Brain 1997; 120: 2059-2069.
5. McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, Lublin FD, McFarland HF, Paty DW, Polman CH, Reingold SC, Sandberg-Wollheim M, Sibley W, Thompson A, van den Noort S, Weinshenker BY, Wolinsky JS,. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol 2001; 50: 121-127.
6. Swanton JK, Rovira A, Tintore M, Altmann DR, Barkhof F, Filippi M, Huerga E, Miszkiel KA, Plant GT, Polman C, Rovaris M, Thompson AJ, Montalban X, Miller DH,. MRI criteria for multiple sclerosis in patients presenting with clinically isolated syndromes: a multicentre retrospective study. Lancet Neurol 2007; 6: 677-686.
7. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, Lublin FD, Montalban X, O'Connor P, Sandberg-Wollheim M, Thompson AJ, Waubant E, Weinshenker B, Wolinsky JS,. Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald criteria. Ann Neurol 2011; 69: 292-302.
8. Bakshi R, Thompson AJ, Rocca MA, Pelletier D, Dousset V, Barkhof F, Inglese M, Guttmann CRG, Horsfield MA, Filippi M,. MRI in multiple sclerosis: current status and future prospects. Lancet Neurol 2008; 7: 615-625.
9. Miller D, Barkhof F, Montalban X, Thompson A, Filippi M,. Clinically isolated syndromes suggestive of multiple sclerosis, part 2: non-conventional MRI, recovery processes, and management. Lancet Neurol 2005; 4: 341-348.
10. Bates D,. Treatment effects of immunomodulatory therapies at different stages of multiple sclerosis in short-term trials. Neurology 2011; 76: S14-S25.
11. Freedman MS,. Long-term follow-up of clinical trials of multiple sclerosis. Neurology 2011; 76: S26-S34.
12. Barkof F, Calabresi PA, Miller DH, Reingold SC,. Imaging outcomes for neuroprotection and repair in multiple sclerosis trials. Nat Rev Neurol 2009; 5: 256-266.
13. Adams CW, Poston RN, Buk SJ, Sidhu YS, Vipond HL,. Inflammatory vasculitis in multiple sclerosis. J Neurol Sci 1985; 69: 269-283.
14. Wakefield AJ, More LJ, Difford J, McLaughlin JE,. Immunohistochemical study of vascular injury in acute multiple sclerosis. J Clin Pathol 1994; 47: 129-133.
15. Holley JE, Newcombec J, Whatmore JL, Gutowski NS,. Increased blood vessel density and endothelial cell proliferation in multiple sclerosis cerebral white matter. Neurosci Lett 2010; 470: 65-70.
16. Roscoe WA, Welsh ME, Carter DE, Karlik SJ,. VEGF and angiogenesis in acute and chronic MOG (35-55) peptide induced EAE. J Neuroimmunol 2009; 209: 6-15.
17. Zaharchuk G,. Theoritical basis of hemodynamic MR imaging techniques to measure cerebral blood volume, cerebral blood flow, and permeability. AJNR Am J Neuroradiol 2007; 28: 1850-1858.
18. Law M, Saindane AM, Ge Y, Babb JS, Johnson G, Mannon LJ, Herbert J, Grossman RI,. Microvascular abnormality in relapsing-remitting multiple sclerosis: perfusion MR imaging findings in normal-appearing white matter. Radiology 2004; 231: 645-652.
19. Ge Y, Law M, Johnson G, Babb JS, Mannon LJ, Grossman RI,. Dynamic susceptibility contrast perfusion MR imaging of multiple sclerosis lesions: characterizing hemodynamic impairment and inflammatory activity. AJNR Am J Neuroradiol 2005; 26: 1539-1547.
20. Adhya S, Johnson G, Herbert J, Jaggi H, Babb JS, Grossman RI, Inglese M,. Pattern of hemodynamic impairment in multiple sclerosis: dynamic susceptibility contrast perfusion MR imaging at 3.0 T. Neuroimage 2006; 33: 1029-1035.
21. Inglese M, Park S-J, Johnson G, Babb JS, Miles L, Jaggi H, Herbert J, Grossman RI,. Deep gray matter perfusion in multiple sclerosis dynamic susceptibility contrast perfusion magnetic resonance imaging at 3 T. Arch Neurol 2007; 64: 196-202.
22. Saindane AM, Law M, Ge Y, Johnson G, Babb JS, Grossman RI,. Correlation of diffusion tensor and dynamic perfusion MR imaging metrics in normal-appearing corpus callosum: support for primary hypoperfusion in multiple sclerosis. AJNR Am J Neuroradiol 2007; 28: 767-772.
23. Haselhorst R, Kappos L, Bilecen D, Scheffler K, Mori D, Radu EW, Seelig J,. Dynamic susceptibility contrast MR imaging of plaque development in multiple sclerosis: application of an extended blood-brain barrier leakage correction. J Magn Reson Imaging 2000; 11: 495-505.
24. Mastorodemos V, Nikolakaki H, Tzagournissakis M, Kotzamani D, Panou T, Spanaki C, Klados G, Maris T, Kontolaimaki E, Psaroudaki K, Chlouverakis G, Georgakakis G, Plaitakis A,. Benign multiple sclerosis in crete. Mult Scler 2010; 16: 701-706.
25. Poser CM,. Onset symptoms of multiple sclerosis. J Neurol Neurosurg Psychiatry 1995; 58: 253-254.
26. Kurtzke JF,. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983; 33: 1444-1452.
27. Fountoulakis K, Iacovides A, Kleanthous S, Samolis S, Kaprinis SG, Sitzoglou K, St Kaprinis G, Bech P,. Reliability, validity and psychometric properties of the Greek translation of the Center for Epidemiological Studies-Depression (CES-D) Scale. BMC Psychiatry 2001; 1: 3.
28. 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.
29. Alsop D,. Perfusion imaging of the brain. In:, Edelman RR, Hesselink JR, Zlatkin MB, Crues JV, editors. Clinical magnetic resonance imaging, 3rd ed. Philadelphia, PA: Saunders Elsevier; 2006. pp 333-376.
30. Welch EB, Felmlee JP, Ehman RL, and, Manduca A,. Motion correction using the K-space phase difference of orthogonal acquisitions. Magn Reson Med 2002; 48: 147-156.
31. Tofts PS,. Modeling tracer kinetics in dynamic Gd-DTPA MR imaging. J Magn Reson Imaging 1997; 7: 91-101.
32. Ostergaard L, Weisskoff RM, Chesler DA, Gyldensted C, Rosen BR,. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages, part 1: mathematical approach and statistical analysis. Magn Reson Med 1996; 36: 715-725.
33. Ostergaard L, Sorensen AG, Kwong KK, Weisskoff RM, Gyldensted C, Rosen BR,. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages, part 2: experimental comparison and preliminary results. Magn Reson Med 1996; 36: 726-736.
34. Calamante F, Gadian DG, Connelly A,. Delay and dispersion effects in dynamic susceptibility contrast MRI: simulations using singular value decomposition. Magn Reson Med 2000; 44: 466-473.
35. Wirestam R, Andersson L, Ostergaard L, Bolling M, Aunola J, Lindgren A, Geijer B, Holtas S, Stahlberg F,. Assessment of regional cerebral blood flow by dynamic susceptibility contrast MR using different deconvolution techniques. Magn Reson Med 2000; 13: 691-700.
36. Jackson A,. Analysis of dynamic contrast enhanced MRI. Br J Radiol 2004; 77: S154-S166.
37. Knutsson L, Stahlberg F, Wirestam R,. Aspects on the accuracy of cerebral perfusion parameters obtained by dynamic susceptibility contrast MRI: a simulation study. Magn Reson Imaging 2004; 22: 789-798.
38. Schneider F, Gur RE, Mozley LH, Smith RJ, Mozley PD, Censits DM, Alavi A, Gur RG,. Mood effects on limbic blood flow correlate with emotional self-rating: a PET study with oxygen-15 labeled water. Psychiatry Res 1995; 61: 265-283.
39. Ibaraki M, Ito H, Shimosegawa E, Toyoshima H, Ishigame K, Takahashi K, Kanno I, Miura S,. Cerebral vascular mean transit time in healthy humans: a comparative study with PET and dynamic susceptibility contrast-enhanced MRI. J Cereb Blood Flow Metab 2007; 27: 404-413.
40. Sicotte NL, Kern KC, Giesser BS, Arshanapalli A, Schultz A, Montag M, Wang H, Bookheimer SY,. Regional hippocampal atrophy in multiple sclerosis. Brain 2008; 131: 1134-1141.
41. Gold SM, Kern KC, O'Connor M-F, Montag MJ, Kim A, Yoo YS, Giesser BS, Sicotte NL,. Smaller cornu ammonis (CA) 2-3/dentate gyrus volumes and elevated cortisol in multiple sclerosis patients with depressive symptoms. Biol Psychiatry 2010; 68: 553-559.
42. Filippi M, Rocca MA,. MRI aspects of the "inflammatory phase" of multiple sclerosis. Neurol Sci 2003; 24: 5275-5278.
43. Sieven NC, Tofts PS, Symms MR, Barker GJ, Thompson AJ, Miller DH,. Quantitative contrast-enhanced MRI to evaluate blood-brain barrier integrity in multiple sclerosis: a preliminary study. Mult Scler 2001; 7: 75-82.
44. Wuerfel J, Bellmann-Strobl J, Brunecker P, Aktas O, McFarland H, Villringer A, Zipp F,. Changes in cerebral perfusion precede plaque formation in multiple sclerosis: a longitudinal perfusion MRI study. Brain 2004; 127: 111-119.
45. Paolillo A, Piattella MC, Pantano P, Di Legge S, Caramia F, Russo P, Lenzi GL, Pozzilli C,. The relationship between inflammation and atrophy in clinically isolated syndromes suggestive of multiple sclerosis: a monthly MRI study after triple-dose Gadolinium DTPA. J Neurol 2004; 251: 432-439.
46. Inglese M, Benedetti B, Filippi M,. The relation between MRI measures of inflammation and neurodegeneration in multiple sclerosis. J Neurol Sci 2005; 233: 15-19.
47. Pathak AP, Schmainda KM, Ward BD, Ward BD, Linderman JR, Rebro KJ, Greene AS,. MR-derived cerebral blood volume maps: issues regarding histological validation and assessment of tumor angiogenesis. Magn Reson Med 2001; 46: 735-747.
48. Plumb J, McQuaid S, Mirakhur M, Kirk J,. Abnormal endothelial tight junctions in active lesions and normal-appearing white matter in multiple sclerosis. Brain Pathol 2002; 12: 154-169.
49. Lassmann H,. Hypoxia-like tissue injury as a component of multiple sclerosis lesions. J Neurol Sci 2003; 206: 187-191.
50. Sun X, Tanaka M, Kondo S, Okamoto K, Hirai S,. Clinical significance of reduced cerebral metabolism in multiple sclerosis: a combined PET and MRI study. Ann Nucl Med 1998; 12: 89-94.
51. De Keyser J, Steen C, Mostert JP, Koch MW,. Hypoperfusion of the cerebral white matter in multiple sclerosis: possible mechanisms and pathophysiological significance. J Cereb Blood Flow Metab 2008; 28: 1645-1651.
52. Rashid W, Hadjiprocopis A, Davies G, Griffin C, Chard D, Tiberio M, Altmann D, Wheeler-Kingshott C, Tozer D, Thompson A, Miller D,. Longitudinal evaluation of clinically early relapsing-remitting multiple sclerosis with diffusion tensor imaging. J Neurol 2008; 255: 390-397.
53. Varga AW, Johnson G, Babb JS, Herbert J, Grossman RI, Inglese M,. White matter hemodynamic abnormalities precede sub-cortical gray matter changes in multiple sclerosis. J Neurol Sci 2009; 282: 28-33.
54. Knutsson L, van Westen D, Petersen ET, Bloch KM, Holtås S, Ståhlberg F, Wirestam R,. Absolute quantification of cerebral blood flow: correlation between dynamic susceptibility contrast MRI and model-free arterial spin labeling. Magn Reson Imaging 2010; 28: 1-7.
55. Roosendaal SD, Moraal B, Vrenken H, Castelijns JA, Pouwels PJ, Barkhof F, Geurts JJ,. In vivo MR imaging of hippocampal lesions in multiple sclerosis. J Magn Reson Imaging 2008; 27: 726-731.
56. Geurts JJ, Bo L, Roosendaal SD, Hazes T, Daniels R, Barkhof F, Witter MP, Huitinga I, van der Valk P,. Extensive hippocampal demyelination in multiple sclerosis. J Neuropathol Exp Neurol 2007; 66: 819-827.
57. Benedict RH, Ramasamy D, Munschauer F, Weinstock-Guttman B, Zivadinov R,. Memory impairment in multiple sclerosis: correlation with deep grey matter and mesial temporal atrophy. J Neurol Neurosurg Psychiatry 2009; 80: 201-206.
58. Papadopoulos D, Dukes S, Patel R, Nicholas R, Vora A, Reynolds R,. Substantial archaeocortical atrophy and neuronal loss in multiple sclerosis. Brain Pathol 2009; 19: 238-253.
59. Ziehn MO, Avedisian AA, Tiwari-Woodruff S, Voskuhl RR,. Hippocampal CA1 atrophy and synaptic loss during experimental autoimmune encephalomyelitis, EAE. Lab Invest 2010; 90: 774-786.